Bioremediation Technologies

Rev Environ Sci Biotechnol (2006) 5:347374 DOI 10.
1007/s11157-006-0004-1
REVIEW PAPER
Bioremediation technologies for treatment of PAH-contaminated soil and strategies to enhance process efciency
S. Venkata Mohan Takuro Kisa Takeru Ohkuma Robert A. Kanaly Yoshihisa Shimizu
Received: 23 February 2006 / Accepted: 19 May 2006 / Published online: 15 July 2006 Springer Science+Business Media B.V. 2006
Abstract The complex and diverse structural congurations of polycyclic aromatic hydrocarbons (PAHs), combined with their low bioavailability, hydrophobic nature, strong sorption phenomena, and high persistence in soil makes the design of effective bioremediation methodologies a challenge. The multi-phasic nature of the bioremediation process, restricted mass transfer and non-availability of degrading soil microora further compound the problem. In this direction, this communication presents a focused review of bioremediation technologies used recently for the treatment of PAH-contaminated soils. The specic roles of important factors affecting bioremediation process efciency are discussed. Finally some of the recently used strategies to enhance bioremediation process efciency,
S. V. Mohan (&) Bioengineering and Environmental Centre, Indian Institute of Chemical Technology, Hyderabad 500 007, India e-mail: vmohan_s@yahoo.com T. Kisa T. Ohkuma Y. Shimizu S. V. Mohan Research Center for Environmental Quality Management, Kyoto University, Otsu, Shiga 520 0811, Japan R. A. Kanaly Department of Technology and Ecology, Graduate School of Global Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
including bioaugmentation, biostimulation, rhizoremediation, the use of chemotaxins, the biomimetic catalytic system approach, and integrated techniques, are reviewed. Keywords Polycyclic aromatic hydrocarbons (PAHs) Bioremediation Technologies Bioavailability Factors Bioaugmentation Biostimulation Bacterial chemotaxins Rhizoremediation Biomimetic catalytic system
Introduction Polycyclic aromatic hydrocarbons (PAHs) represent a large and diverse group of organic molecules having a broad range of properties, differing in molecular weight, structural conguration, water solubility, number of aromatic rings, volatility, sorption coefcients, etc. (Harayama 1997; Kanaly and Harayama 2000; MaliszewskaKordybach and Smreczak 2000; Harmsen 2004). Anthropogenic sources like gasoline and diesel fuel combustion, oil spills, former gas plant facilities, etc., contribute PAHs to the environmental matrix (Juhasz and Naidu 2000; Kanaly and Harayama 2000; Meckenstock et al. 2004; Johnsen et al. 2005) and their ubiquitous distribution, environmental persistence and potentially deleterious effect on human health have resulted in an increasing interest by the research commu-
123
348
Rev Environ Sci Biotechnol (2006) 5:347374
nity. In many cases, their non-environmentally friendly nature and cost of treatment offsets the application of commonly used remediation technologies such as land removal, incineration or land lling. Considering these circumstances, bioremediation is gaining wider approval as a feasible alternative treatment technology for the remediation of soils contaminated with PAHs. Indeed, bioremediation is considered to be a safe, efcient, eco-friendly and economic means of removing pollutants from contaminated soil without simply enacting transfer to another medium. Reports pertaining to bioremediation studies of PAH-contaminated soils have increased over the last 5 years. Generally, biological degradation is the primary dissipation mechanism for most organic pollutants in the soil environment, but the activity of degrading microorganisms is dependent upon many factors, including contaminant uptake and bioavailability, concentration, toxicity, mobility, access to other nutrients, and activated enzymes (Cerniglia 1984, 1992). Low bioavailability and toxicity, non-uniform spatial distribution of microorganisms and pollutants, retardation of substrate diffusion by the soil matrix, capability of microbial metabolism, etc., are factors which control the bioremediation efciency of PAHs in the soil matrix. In this realm, additional strategies are being integrated into the bioremediation process to enhance bioremediation process efciency. The major aim of this communication is to review the bioremediation technologies used for PAH-contaminated soils while providing emphasis on the factors inuencing the process efciency. Finally the paper discusses some of the more recently used strategies to enhance bioremediation process efciency.
Bioremediation technologies The scientic literature for the past half decade has documented a considerable number of bioremediation studies on PAH-contaminated soil employing various remediation technologies such as solid phase treatment, land treatment/farming, composting, bioreactors, phytoremediation, enzyme catalyzed bioremediation and combined
methods (chemical pre-treatment followed by bioremediation), in addition to the application of strategies such as biostimulation, microbial adaptation, bioaugmentation, bacterial chemotaxis, etc., for enhancing bioremediation rates. Biostimulation requires adjustments to the site (contaminated soil or water) in order to provide bacterial communities with a favorable environment in which they can effectively degrade contaminants. In cases where natural communities of degrading bacteria are present in low numbers or even absent, bioaugmentation, i.e., the addition of contaminant-degrading organisms, can speed up the degradation process (Van Limbergen et al. 1998; Cunningham et al. 2004). The property of bacterial mobility under the inuence of a chemical gradient, either towards (positive) or away (negative) from the gradient to found optimum conditions for their growth and survival which is called as bacterial chemotaxis (Pandey and Jain 2002), can be positively applied to enhance bioremediation in soil matrix. The process of microbial adaptation is a process that enhance native microora metabolic capability by preexposure of soils to contaminant concentrations greater than the background. Various technologies reported in the literature for the bioremediation of PAH-contaminated soil in the past ve years are consolidated and shown in Table 1. Several researchers studied the efciency of solid phase treatment for the remediation of PAH-contaminated soil employing natural attenuation (Guerin 2000; Taylor and Jones 2001; Chang et al. 2002; Gogi et al. 2003; Xu et al. 2005a, b; Trindade et al. 2005), ex situ methods (Chang et al. 2002; Boopathy 2003; Oleszczuk and Baran 2003; Gong et al. 2005; Ambrosoli et al. 2005; Coulon et al. 2005; Macleod and Semple 2005; Sabate et al. 2006) and land farming (Betancur-Galvis et al. 2006) at both laboratory and eld scales. Some of these studies also elucidated the effects of biostimulation (Taylor and Jones 2001; Chang et al. 2002; Delille et al. 2004; Xu et al. 2005a, b; Coulon et al. 2005; Gong et al. 2005; Trindade et al. 2005; Sabate et al. 2006), bioaugmentation (Zheng and Obbard 2002; Garon et al. 2004; Venkata Mohan et al. 2004b; Trindade et al. 2005; Heinaru et al. 2005), co-substrate addition (Chang et al. 2002; Gong
123
Table 1 Bioremediation technologies for the bioremediation of PAH-contaminated soil Conditions Aerobic Aerobic Heavy vehicle maintained facility soil Coal tar-contaminated soil Source of contaminant Reference Guerin (2000) Taylor and Jones (2001)
Process
Method
Solid phase treatment/ Natural attenuation/ Land farming/Land treatment PAHs-contaminated soil (synthetic)
In situ In situ eld study, biostimulation with biodiesel and nitrogen and phosphorus source Ex situ, biostimulation with nutrients, municipal sewage and renery oil sludge
Chang et al. (2002)
In situ Ex situ
Oil eld-contaminated soil Diesel fuel-contaminated sediments
Gogoi et al. (2003) Boopathy (2003)
In situ Aerobic Aerobic Aerobic Aerobic Aerobic
Anaerobic, sulphate- and nitrate-reducing conditions Aerobic Anaerobic, mixed electron acceptor conditions Aerobic Aircraft oil-contaminated soil Wood treatment facility soil PAH-contaminated saline alkaline soil Oil contaminated sediments Manufactured gas plant soil Oil-contaminated soil Biphenyl, uorene, phenanthrene, pyrene contaminated soil
Ex situ using land treatment units In situ
Oleszczuk and Baran (2003) Hansen et al. (2004) Betancur-Galvis et al. (2006) Xu et al. (2005a, b) Gong et al. (2005) Trindade et al. (2005) Ambrosoli et al. (2005)
In situ, eld trial, biostimulation with slow releasing fertilizer and chitosan Ex situ, sunower oil and nutrient addition In situ, natural attenuation, bioaugmentation and biostimulation Ex situ
Ex situ, nutrients Aerobic Aerobic Aerobic Aerobic Aerobic Aerobic
Anaerobic, denitrifying conditions Aerobic
Coulon et al. (2005)
Ex situ, adaptation
Diesel contaminated sub-antractic soil (synthetic) Pyrene-contaminated soil Wood treatment facility soil PAH-contaminated soil PAH-contaminated alkaline soil Coal tar contaminated soil Pyrene and benzo[a]pyrene contaminated soil (synthetic) Pyrene-contaminated soil
Macleod and Semple (2005) Sabate et al. (2006) Lau et al. (2003) Moretto et al. (2005) Antizar-Ladislao et al. (2005a, b and 2006) Haderlein et al. (2005) Liste and Alexander (2000) 349
Composting
Phytoremediation/ Rhizoremediation
Ex situ, biostimulation with aeration and soil water adjustment Ex situ composting with spent mushroom Ex situ, composting with soot waste Ex situ, in vessel composting with green waste, pilot scale study Ex situ composting with maple leaves and alfalfa In situ, nine plant species
123
350
Table 1 continued Conditions Joner et al. (2001) Source of contaminant Reference
123
Ortega-Calvo et al. (2003) Verveke et al. (2003) Johnson et al. (2004) Huang et al. (2004) Parrish et al. (2004 and 2005) Chyrene and dibenz [a,h]nthracene contaminated soil PAHs-contaminated soil PAHs-contaminated soil Chrysene contaminated soil Creosote contaminated soil Manufactured gas plant site Benzo[a]pyrene Rentz et al. (2005) PAHs-contaminated soil Johnson et al. (2005) Aerobic Aerobic Liste and Prutz (2006) Parrish et al. (2005) Xu et al. (2006) Former manufactured gas plant site soil Manufactured Gas Plant site soil Phenanthrene and pyrene contaminated soil Diesel oil-contaminated soil Coal tar-contaminated soil PAHs-contaminated soil Aerobic Aerobic Aerobic Kaimi et al. (2006) Canet et al. (2001) Zheng and Obbard (2002) Garon et al. (2004) Fluorenecontaminated soil Anthracene-contaminated soil (synthetic) Coal tar-contaminated soil Venkata Mohan et al. (2004b) Lee et al. (2001)
Process
Method
Mixed sward of clover and ryegrass
Bacterial chemotaxins Willo stands Mixed grass legume system with microbial inoculum Multiple process phytoremediation system Rhizodegradtion using Tall fescue (Festuca arundinacea Schreb) and yellow sweet clover (Melilotus ofcinalis Lam) Plant root extracts of osage orange (Maclura pomifera), hybrid willow (Salix albaXmatsydana), kou (Cordia subcordata), plant root exudates of white mulberry (Morus alba) Mixed ryegrass (Lolium perenne) and white clover (Trifolium repens) sward together with a rhizobial inoculum (Rhizobium leguminosarum) Greenhouse pot
Earthworm
Enzyme-mediated treatment
Bioreactors
Three plant species (maize, ryegrass and white clover) Ryegrass White rot fungus and native soil microora Soil slurry bioreactor (augmented with fungus Phanerochaete chrysosporium) Soil slurry bioreactor (augmented with fungus Absidia cylindrospora) Ex situ, augmented with laccase from Pleurotus ostreatus 1804 Ex situ, soil slurry bioreactor, solvent pre-treatment
Table 1 continued Conditions Aerobic Aerobic Aerobic Aerobic PAHs-contaminated soil Phenanthrene-contaminated soil PAHs-contaminated soil PAHs-contaminated soil Kim et al. (2001a, b) Villemur et al. (2000) Woo et al. (2001) Zheng and Obbard (2002) Boopathy (2003) Source of contaminant Reference
Process
Method
Ex situ, soil slurry bioreactor, non-ionic surfactant (Brij30) addition Ex situ, soil slurry bioreactor, silicone oil Ex situ, soil slurry bioreactor Ex situ, soil slurry bioreactor (augmented with fungus Phanerochaete chrysosporium) Ex situ, soil slurry bioreactor Anaerobic, mixed electron acceptor conditions Aerobic Diesel fuel-contaminated sediments Creosote-contaminated soil Phenanthrene-contaminated soil Fluorene-contaminated soil Aerobic Aerobic
USEPA (2003) Seung et al. (2004a, b) Garon et al. (2004)
Aerobic Aerobic Aerobic
Fluorene-contaminated soil Phenanthrene- contaminated soil Diesel oil-contaminated soil
Garon et al. (2004) Woo et al. (2004) Biswas et al. (2005)
Ex situ pilot scale study, soil slurry bioreactor Ex situ, soil slurry bioreactor Ex situ, soil slurry bioreactor (augmented with fungus Absidia cylindrospora) Ex situ, soil slurry bioreactor, addition of maltosyl cyclodextrin Ex situ, soil slurry bioreactor Ex situ, soil slurry bioreactor, using spill clean up sorbents (peat sorb and spill sorb) Ex situ, soil slurry bioreactor Aerobic, sulfur oxidizing conditions Anaerobic PAHs-contaminated sediments
Lei et al. (2005) Naphthalene, acenaphthene, pyrene and benzo[b] fluoranthene contaminated soil Diesel fuel-contaminated sediments Koran et al. (2001)
Ex situ, soil-solvent washing followed by anaerobic treatment of the extract by uidized bed conguration Ex situ, soil column bioreactor
Boopathy (2004)
Ex situ, soil column bioreactor
Ex situ, soil column bioreactor Aerobic Aerobic Aerobic
Anaerobic, mixed electron acceptor conditions Anaerobic, sulphate reducing conditions Aerobic
Coal derived hydrocarbons-contaminated soil Coal derived hydrocarbons-contaminated soil Crude oil-contaminated soil Pyrene-contaminated soil Crude oil-contaminated soil
Kuwano and Shimizu (2006) Kumada et al. (2005) Baptista et al. (2005) Bordas et al. (2005) Wrenn et al. (2006)
Ex situ, soil column bioreactor (xed) Ex situ, soil column bioreactor, biosurfactant addition Ex situ, continuous-ow beach microcosm reactor
351
123
352
Table 1 continued Conditions Aerobic Aerobic Coal tar-contaminated soil PAHs-contaminated sand Choi et al. (2001) Lee et al. (2001) Source of contaminant Reference
123
Anaerobic Koran et al. (2001) Aerobic Naphthalene, acenaphthene, pyrene, and benzo(b)uoranthene contaminated soil Creosote- contaminated soil Huang et al. (2004) Aerobic Aerobic Creosote-contaminated soil PAHs-contaminated soil Goi and Trapido (2004) Kulik et al. (2006) Aerobic Aerobic aerobic PAHs-contaminated soil Diesel oil-contaminated soil Diesel oil-contaminated soil Johnson et al. (2005) Ahn et al. (2005) Biswas et al. (2005) Aerobic Phenanthrene-contaminated soil OMahony et al. (2006)
Process
Method
Combined treatment
Ex situ, ozone oxidation integrated bioremediation Ex situ, solvent pre-treatment integrated soil slurry phase bioremediation Ex situ, soil-solvent washing and anaerobic treatment of the extract Multiple process integration (physical, photochemical, bioremediation and Phytoremediation) Ex situ, Fenton/ozone oxidation integrated bioremediation Ex situ, combined chemical oxidation (ozone and Fenton type treatment) integrated with bioremediation Ex situ combined treatment with ryegrass, white clover sword and rhizobial inoculum Ex situ, pre-ozonation integrated with bioremediation Ex situ, using site spill clean up sorbents (peat sorb and spill sorb) along with soil slurry phase bioremediation Ex situ, ozone oxidation integrated bioremediation
353
et al. 2005) and adaptation (Macleod and Semple 2005) on bioremediation process efciency. Comparatively, few solid phase bioremediation studies that focused on the anaerobic microenvironment by employing different electron acceptor conditions were reported (Chang et al. 2002; Boopathy 2003; Ambrosoli et al. 2005). Land farming Among solid phase treatment technologies, land farming (LF) has a distinctive advantage for stimulating the native soil microora that are enriched in the soil by the presence of contaminants but that are constrained in their degradation capability by limiting factors such as inadequate aeration, poor contact of the microorganisms with the contaminants and insufcient nutrients (Hansen et al. 2004). Normally, traditional agricultural procedures are used to create mixing and aeration (tilling, bulking) and to provide moisture (irrigation) and nutrients (fertilizer; FRTR, 1998). LF is one of the accepted remediation processes by the US EPA for the remediation of wood treatment facility sites (US EPA 1995). The operation and management costs are a major portion of the overall costs of LF bioremediation. Hansen and coworkers (2004) investigated the bioremediation of contaminated soil from a wood treatment facility using two pilot-scale land-treatment units (LTUs) and evaluated the efcacy of different cultivation strategies (traditional LF practice compared with gas-phase composition (oxygen concentration) based cultivation) and maintenance schedules (intensive-treatment and nonintensive treatment). Although different microbial populations developed in the two LF units, the two strategies resulted in similar contaminant degradation proles. LF, as with other solid-phase treatment technologies, often demonstrates a biphasic behavior in terms of contaminant degradation patterns: an initial rapid reduction followed by a slower rate of degradation (Hansen et al. 2004). Composting Composting technology involves the addition of organic bulking agents to the compost mixture
which facilitates an increase in porosity leading to effective air ow and serves as a source of easyto-assimilate carbon for biomass growth (Eweis et al. 1998; Antizar-Ladislao et al. 2004). Energy released during organic degradation results in temperature elevation facilitating that the system pass through four major microbiological phases (mesophilic, thermophilic, cooling and maturation) (Antizar-Ladislao et al. 2005a). The mesophilic stage normally has the highest microbial diversity while the thermophilic stage is characterized by spore-forming bacteria and thermophilic fungi. Microbial recolonisation during the cooling phase is characterized by the appearance of mesophilic fungi whose spores withstand the high temperatures of the thermophilic stage. In the nal compost stage (maturation), most digestible organic matter was found consumed by the microbial population and the composted material is considered stable (Sela et al. 1998). Composting has been demonstrated to be effective in biodegrading PAHs at both laboratory and eld scales using different types of compost bulking agents such as spent mushroom (Lau et al. 2003), soot waste (Moretto et al. 2005), green wastes (Antizar-Ladislao et al. 2005a) and maple leaves and alfalfa (Haderlein et al. 2005). Lau and co-workers (2003) used spent mushroom compost as a waste byproduct of the mushroom industry as a bulking agent (5%) to bioremediate PAH-contaminated soil. Complete degradation of individual naphthalene, phenanthrene, benzo[a]pyrene and benzo[g,h,i]perylene was observed in 48 h at 80C. Haderlein and co-workers (2005) studied the effects of composting or simple addition of compost to soil during the mineralization of pyrene and benzo[a]pyrene by addition of maple leaves and alfalfa. It was reported that neither composting nor the addition of compost had any effect on benzo[a]pyrene mineralization. In contrast, the pyrene mineralization rate increased dramatically with the amount of time that the soil had been composted (more than 60% mineralization after 20 days). Antizar-Ladislao and coworkers (2005b, 2006) used in-vessel composting technology for the remediation of coal tarcontaminated soil and optimized the soil composting temperature at 38C for the most effective degradation.
123
354
Phyotremediation Several studies have showed the suitability of phytoremediation to soils polluted by PAHs (Liste and Alexander 2000; Joner et al. 2001; Ortega-Calvo et al. 2003; Verveke et al. 2003; Johnson et al. 2004, 2005; Huang et al. 2004; Parrish et al. 2005; Haderlein et al. 2005; Liste and Prutz 2006; Xu et al. 2006). Phytoremediation, or rhizoremediation, is the use of plants and/or the associated rhizosphere to decontaminate polluted sites, and is considered today to be a realistic, low-cost alternative for treating extensive areas of pollution by organic chemicals (Susrala et al. 2002; Parrish et al. 2005). This technology is based on the catabolic potential of root-associated microorganisms, which are supported by the organic substrates in root excretions and by a favorable microenvironment in the rhizosphere. According to Parrish et al. (2005), plants may serve multiple roles inuencing the fate of organic contaminants in soil by (1) simultaneously promoting the degradation of the available fractions via stimulation of microbial activity, (2) increasing the number of sites in the organic matrix available for PAH adsorption and eventual binding by contributing root matter to the soil organic matter (SOM), and/or (3) exuding compounds that increase the bioavailability of the contaminants. Phytoremediation may largely result from the enhanced degradation of organic compounds in the rhizosphere as a result of the higher densities and greater activities of microorganisms than in the surrounding soil (Cunningham et al. 1996; Ferro et al. 1994). Plants enhance the bioavailability of contaminants due to the function of root growth and their subsequent penetration through the soil exposing entrapped contaminants that may have been previously inaccessible, thereby increasing their availability to degradation (Parrish et al. 2005). The advantages of phytoremediation compared with other approaches are that it preserves the natural structure and texture of the soil, that energy is derived primarily from sunlight, that high levels of microbial biomass in the soil can be achieved, that it is low in cost and that it has the potential to be rapid (Huang et al. 2004).
Liste and Alexander (2000) studied the capability of nine plant species to promote the degradation of pyrene in soil and reported higher degradation rates in vegetated soil. Xu et al. (2006) studied the performance of three plant species (maize, ryegrass and white clover) for phenanthrene and pyrene removal and concluded that the presence of vegetation signicantly enhanced the dissipation of phenanthrene and pyrene in the soil environment. Approximately 92% of phenanthrene and 88% of pyrene was found to be removed from soils planted with maize. Combined plant-cultivation (maize, ryegrass and white clover) showed signicantly enhanced degradation rates (phenanthrene, 98% and pyrene, 95%) in soils. Liste and Prutz (2006) investigated the potential of 13 plant species in greenhouse pot experiments in a long-term contaminated soil from a former manufactured gas plant site, to promote the proliferation of total and aromatic ring dioxygenase-expressing bacteria (ARDB) in the root zone and to foster the biodegradation of PAHs. They concluded that the plants enhanced the biological availability of initially non-extractable molecules. The differences in PAH concentration between the unplanted and the planted soil indicated that the presence of plant roots, in addition to the passage of time, contributed to a reduction in the bioavailability of target PAHs (Parrish et al. 2005). Vervaeke et al. (2003) made a eld trial to assess the impact of planting a willow stand (Salix viminalis L. Orm) on the dissipation of PAHs in dredged sediment and observed most pronounced degradation in the root zone of the stand. They concluded that the establishment of fast-growing willow stands on land can result in the revaluation of contaminants leading to the possibility for phytoremediation (Vervaeke et al. 2003). Root exudates are found to enhance the desorption of contaminants from the soil matrix. Plant- and root-associated microorganisms have been shown to secrete enzymes and exudates that act as surfactants and increase the available contaminant concentration in soil (Fava et al. 2004; Bogan et al. 2003). Plants enhance the remediation of soils containing organic pollutants by various processes (Shimp et al. 1993; Cunningham et al. 1996, 2004; Liste and Alexander 2000).
123
355
Phytoremediation may largely result from the enhanced degradation of organic compounds in the rhizosphere as a result of the higher densities and greater activities of microorganisms than in the surrounding soil (Cunningham et al. 1996). In addition, plant transpiration may result in the transport of contaminants dissolved in the water from areas outside the root zone towards the root (Ferro et al. 1994). Remediation of contaminated soil therefore may be enhanced by plants because they function like a solar driven pump that has degradative activity in the rhizosphere (Cunningham et al. 1996). Recent studies suggest that the pump and- treat concept that has been hypothesized applies even to hydrophobic compounds such as PAHs (Liste and Alexander 2000). Bioreactors Comparatively extensive work was documented in the literature pertaining to the application of bioreactor technology for the remediation of PAH-contaminated soil (Table 1). Two reactor congurations, namely soil column bioreactors and a soil slurry phase bioreactor were mostly studied. Soil column bioreactors bring about effective degradation of soil bound contaminants by facilitating increased contact with the water phase, which carries nutrients, additional carbon sources and oxygen under controlled and optimized conditions (Kumada et al. 2005). In contrast, the soil slurry phase system uses a liquid slurry treatment mechanism facilitating effective contact of the contaminant with the microora (Venkata Mohan et al. 2004a and 2006). Soil slurry has shown to signicantly enhance both the initial rates and overall extents of mineralization (White et al. 1999; Doick and Semple 2003). The soil content in the slurry signicantly alters the distribution of target compounds between the water and soil, particularly in systems with different mass transfer properties. Reactors utilize naturally occurring bacteria (native soil microora) or inoculated strains having specic metabolic capabilities to metabolize contaminants present either in the solid or liquid phases under optimum environmental conditions. Compared to solid phase
systems, bioreactors facilitate effective degradation of contaminants in less time. Several research studies reported application of soil slurry phase bioremediation for the remediation of PAH-contaminated soil by adopting various process variations under aerobic (Kim et al. 2001a, b; Lee et al. 2001; US EPA 2003; Seung et al. 2004a, b; Garon et al. 2004; Woo et al. 2004; Biswas et al. 2005; Lei et al. 2005) and anaerobic (Boopathy 2003; Kuwano and Shimizu 2006) microenvironments. The process variations integrated in slurry phase operation include: the use of prior solvent pre-treatment (Lee et al. 2001), the use of non-ionic surfactants (Kim et al. 2001a, b), bioaugmentation with fungal strains (Garon et al. 2004), biostimulation with the addition of carbon sources (Garon et al. 2005), the use of adsorbents (Biswas et al. 2005) and the use of sulfur-oxidizing conditions (Lei et al. 2005). The US EPA (2003) under the superfund innovative technology evaluation (SITE) program, evaluated the performance of soil slurry phase reactors for the treatment of creosote contaminated soil at the pilot scale level employing a 30% soil slurry, indigenous soil microbiota, nitrogen supplementation in the form of ammonia, and nutrients (potassium, phosphate, magnesium, calcium and iron). The study demonstrated the effectiveness of slurry phase bioreactor technology in treating PAH-contaminated soil to levels below regulatory standards. The main advantage of the slurry system as per the EPA includes on-site treatment and often, in situ treatment. Lei et al. (2005) revealed the importance of indigenous bacteria involved in natural sulfur cycling by determining the degradation behavior of PAHs under sulfate oxidizing conditions. Reduced sulfur compounds present in the sediment caused rapid oxygen depletion due to the extensive activities of sulfur-oxidizing bacteria and resulted in a dramatic pH drop. Once the oxygen depletion and acidication problems were solved, substantial removal of two-, three-, four-, and vering PAHs were achieved aerobically, though the extent of degradation was smaller than what was reported for freshly spiked PAHs. However, under denitrifying conditions, PAH degradation was not observed, while the complete denitrication of
123
356
nitrate to nitrogen occurred stoichiometrically with a concomitant increase in sulfate concentration, indicating the dominance of autotrophic denitriers. Seung et al. (2004a, b) proposed that a high mass transfer rate with a high input of energy might not always be an effective condition for rapid biodegradation when using the technology of slurry-phase bioremediation and indicated the requirement of a lower mass transfer rate, or shear stress, which might be more favorable for cell growth and subsequent biodegradation. The ndings from their study suggest that mild operating conditions could be of benet to the treatment of contaminated soils with the advantages of low energy cost and rapid biodegradation. Such mild conditions can be achieved by rotating a drum bioreactor (Woo and Park 1999). Conventional slurry phase bioreactors use impellers to suspend soil particles and their mixing is more rigorous than shaking. Furthermore, the effectiveness of the system with low shear stress was increased when the soil content was increased. Additionally, a number of studies that employed soil column bioreactors congured for the bioremediation of PAH-contaminated soils under aerobic (Baptista et al. 2005; Bordas et al. 2005; Kumada et al. 2005; Ohkuma et al. 2006) and anaerobic (Boopathy 2004; Kuwano and Shimizu 2006) conditions have been reported.
Problems associated with the bioremediation process Bioremediation of PAHs in contaminated soil is considered to be a complex phenomenon due to the toxic and hydrophobic nature of the contaminants, soil composition, microbial environment heterogeneity, the multi phasic nature of the bioremediation process and the environmental factors governing the process. Some factors will alter the rate of microbial uptake and metabolism (the intrinsic activity of the cell) and other factors change the rate of contaminant transport to the microorganisms (bioavailability) (Bosma et al. 1997; Tang et al. 2005). According to Semple and co-workers (2004), bioavailability actually describes two distinct fractions: (i) bio-available (that compound which is interacting with biota at
a given moment in time) plus and (ii) bioaccessible (encompasses what is bio-available now plus what is potentially bio-available). Major factors that have a signicant inuence on bioremediation process efciency are presented in the Table 2. Tang et al. (2005) suggested that in view of the complex nature of the bioremediation process, especially in the soil matrix, a proper optimization of factors is essential to advance its efciency. They in turn carried out studies to investigate ways to optimize such factors for enhancing PAH bioremediation efciency in soil by employing the published degradation data using a multiple linear regression approach. The proceeding section of the review discusses some of the strategies applied to enhance bioremediation process efciency for decontaminating PAHcontaminated soil. The role of bioavailability on the microbial metabolism and mass transfer with respect to PAH bioremediation in soils was reported (Juhasz and Naidu 2000; Doick and Semple 2003; Johnsen et al. 2005; Tang et al. 2005; Sabate et al. 2006; Sartoros et al. 2005; Semple et al. 2006; Ohkuma et al. 2006). Bioavailability of contaminants followed by contaminant mass transfer and subsequent metabolism are the factors believed to control the overall bioremediation efciency in the soil matrix especially in regard to hydrophobic contaminants such as PAHs. Ultimate bioremediation efciency will depend on the extent of the bioavailability of the contaminant, its mass transfer rate and subsequent metabolism by the microora. It is well known that the bioavailability of contaminants is inuenced by many factors including chemical structure, molecular weight and toxicity, and soil properties, including soil texture, composition, water content, pH and physical structure. Additionally, physico-chemical interactions of PAHs with soil and environmental factors, such as temperature and moisture inuence the rate and extent of biodegradation (Guerin 1999; Sijm et al. 2000; Johnsen et al. 2005). The problems associated with PAH-bioremediation in soil microcosms can be broadly segregated into four interrelated categories: contaminant associated, soil associated, microbial associated and bioremediation system associated (Fig. 1).
123
Rev Environ Sci Biotechnol (2006) 5:347374 Table 2 Factors inuencing the bioremediation of PAHs in contaminated soils Factors pH Inuence Bioavailability Mass transfer Microbial metabolism rate Bioavailability Mass transfer Microbial metabolism rate Bioavailability Microbial metabolism rate Bioavailability Microbial metabolism rate References Tang et al. (2005); Betancur-Galvis et al. (2006); Moretto et al. (2005) Namkoong et al. (2002); Feitkenhauer et al. (2003); Tang et al. (2005); Coulon et al. (2005); Sartoros et al. (2005) Johnsen et al. (2005); Tang et al. (2005); Juhasz and Naidu (2000); Semple et al. (2006)
357
Temperature
Microora Electron acceptor
Juhasz and Naidu (2000); Boopathy (2003 and 2004); Doick and Semple (2003); Ambrosoli et al. (2005); Johnsen et al. (2005); Tang et al. (2005); Sabate et al. (2006); Sartoros et al. (2005); Tang et al. (2005); Kuwano and Shimizu (2006); Semple et al. (2006); Ohkuma et al. (2006) Kanaly and Harayama (2000); Taylor and Jones (2001); Samanta et al. (2002); Gong et al. (2005); Xu et al. (2005a, b); Johnsen et al. (2005); Meckenstock et al. (2004) Taylor and Jones (2001); Chang et al. (2002); Tang et al. (2005); Coulon et al. (2005); Betancur-Galvis et al. (2006); Wrenn et al. (2006); Semple et al. (2006) Juhasz and Naidu (2000); Taylor and Jones (2001); Chang et al. (2002); Canet et al. (2002); Lau et al. (2003); Moretto et al. (2005); Antizar-Ladislao et al. (2005a and 2006); Haderlein et al. (2005); Garon et al. (2004); Johnsen et al. (2005) Maliszewska-Kordybach and Smreczak (2000); Johnsen et al. (2005); Pan et al. (2006) Juhasz and Naidu (2000); Johnsen et al. (2005); Tang et al. (2005)
Microenvironment
Microbial metabolism rate
Nutrients
Co-substrate
Soil properties Contaminant characteristics
Bioavailability Mass transfer Bioavailability Mass transfer Microbial metabolism rate
Contaminated associated PAHs are composed of fused, aromatic rings whose biochemical persistence arises from dense clouds of p electrons on the ring structures which makes them resistant to nucleophilic attack (Johnsen et al. 2005). They possess physical properties, such as low aqueous solubility and high solidwater distribution ratios, which stand against their ready microbial utilization. While aqueous solubility is a main structural determinant in the biodegradation of PAHs, molecular stability is also important (Guerin 1999). Stability is indicated by the ring arrangement, linear being the most unstable and angular the most stable. This stability can be quantied by the parameters of bond localization energy (BLE). BLE effects ring opening, dictates where on the molecule
oxidation is likely to occur, and the ionization potential. The aqueous solubility, and as a consequence, the bioavailability of PAHs decrease almost logarithmically with increasing molecular mass (Johnsen et al. 2005). In general, biotic mechanisms are responsible for removal of PAHs containing more than 3-rings and volatilization is important only for 2-ring compounds such as naphthalene and 1-methylnaphthalene (Park et al. 1990). Bioremediation rates of PAHs in soil have been shown to decrease with increase in PAH residence time (aging) (Hatzinger and Alexander 1995). The partitioning (Pignatello and Xing 1996), adsorption (Weber and Huang 1996), chemisorption (Maruya et al. 1996), diffusion, dissolution (Ehlers and Luthy 2003), and covalent binding (Bollag 1992) between PAHs and SOM
123
358
Contaminant associated
Physical and chemical characteristics, composition, toxicity
Mass Transfer
Soil associated
Physical and chemical characteristics, soil composition, native soil microflora availability and its efficiency to degrade contaminants
Microbial metabolism
Microbial associated
Native soil microflora availability, survival in presence of contaminant, efficiency to degrade contaminants
Bioremediation system associated

System configuration, operation microenvironment, operation conditions such as temperature, pH, contaminant concentration, nutrients, co-substrate, electron acceptor, moisture content, etc.
Bioavailability
Fig. 1 Factors associated with the bioremediation efciency of PAH-contaminated soil
are believed to be responsible for the decline in their degradation over time. Aging facilitates movement of a contaminant into soil micropores or into the SOM leading to the transformation and/or incorporation of pollutants into stable soil solid phases (Ehlers and Luthy 2003). This process limits the release of PAHs into the bulk liquid phase, making them inaccessible to microorganisms, thus decreasing biodegradation rates (Willumsen and Karlson 1997; Hatzinger and Alexander 1999). Soil associated The biodegradation potential of hydrocarbons is not only dened by their chemical composition, but also by the biological, physical and chemical characteristics of the soil environment (BetancurGalvis et al. 2006). The interactions are considered to be the major rate-limiting factors in eld scale applications. PAHs may be strongly adsorbed onto soil particles, especially clays (Luthy
et al. 1997; White et al. 1997) and desorption of PAHs from soil is considered to be a controlling factor in their biodegradation (Hansen et al. 2004). Low proportions of clay and silt in soil have been correlated to higher PAH bioavailability. Furthermore, partitioning of PAHs into organic matter in soil has been suggested as a mechanism of sequestration by which the PAHs adsorb rapidly to the external surfaces of the soil and then slowly partition into the interior regions of the solid organic matter particles. Due to high hydrophobicity and soil water distribution ratios, PAHs tend to interact with non-aqueous phases and SOM. As a consequence, they become potentially unavailable for microbial degradation due to their limited bioavailability as only small fractions of these compounds occur in the bioavailable water-dissolved state (Johnsen et al. 2005). Additionally, the rate of degradation of hydrocarbons and the total amount mineralized will vary depending upon the soil type (Davis and Madsen 1996).
123
359
Microbial associated The rate at which microbial cells can convert chemicals during bioremediation processes depends on the rate of uptake and metabolism (the intrinsic activity of the cell) and the rate of transfer to the cell (mass transfer) (Bosma et al. 1997). Studies have shown that bacterial degradation is altered greatly by the physical and chemical features of the heterogeneous microbial environment (Tang et al. 2005). Microbial ecology, system microbiology (presence of co-substrates, genetics of the relevant organisms and enzyme stability and activity), process operation conditions (microenvironment and conguration) and the presence/absence of indigenous activity will signicantly govern the overall bioremediation process efciency. The efciency of degradation is often seriously impeded by two factors: poor accessibility of lipophilic compounds to microorganisms and the toxic effects of substrates upon the microorganism (Garon et al. 2004). Bioavailability is driven by mass transfer of the contaminant from the soil phase to the solution phase (Cuypers et al. 2002; Reid et al. 2000). Contrary to studies suggesting that adsorbed contaminants are not bioavailable, recent studies indicate that soil microorganisms may be capable of degrading non-desorbable compounds (Guerin et al. 1992; Guerin and Boyd 1997; Ortega-Calvo and Saiz-Jimenez 1998; Park et al. 2001; Tang et al. 1998). Park et al. (2001) evaluated the substrate depletion of non-desorbable naphthalene and found that this fraction, though unable to be extracted using exhaustive aqueous solutions, was bioavailable to bacteria. Some microbial species may be capable of overcoming the binding that results in contaminant sequestration or they may produce compounds, such as enzymes, surfactants, and emulsiers, that can enhance desorption, giving them an advantage over those without these abilities (Alexander 2000). Remediation system associated Additionally, increased microbial conversion capacities do not necessarily lead to higher biotransformation rates when mass transfer is the
limiting factor (Bosma et al. 1997). PAHs are poorly water soluble and heterogeneously distributed on soils and may be absorbed inside of organic particles, located in small pores that are inaccessible for bacteria, or otherwise occluded by the multitude of solid soil constituents (Johnsen et al. 2005). Bacterial cells are generally excluded from pores smaller than about 0.20.8 lm, and in addition, predation is believed to reduce bacterial biomass in pores, thereby restricting bacterial mobility (Postma and van Veen 1990; Harms and Bosma 1997). Consequently, a large fraction of PAH-degrading bacteria in soil are expected to be physically separated from PAH sources and therefore will depend on diffusive transport of PAHs from the sources to the cells (Harms and Bosma 1997). Mixing does not occur well in soil and the effective diffusion of molecules in soil may be orders of magnitude lower than in water, since diffusion is retarded by the solid phases, dead-end pores, and the high tortuosity of the system. In soil, as opposed to well mixed aqueous systems, substrate consumption leads much faster to mass transferlimited conditions as the number of cells increases. Therefore PAH-degrading populations in soil are probably mostly not growing, but rather are in a pseudo-stationary phase where transient growth only replaces decaying cells until the habitats mass transfer-controlled carrying capacity is reached again (Johnsen et al. 2005). Mass transfer phenomena depend on diffusion, which further links with the thickness of the boundary layer related to the size and shape of the molecule and the shaking velocity (Mulder et al. 1998). The smaller the crystals and the higher the shaking velocity, the thinner is the boundary layer and the higher the PAH-ux from solid form to the bulk liquid (Johnsen et al. 2005). In studies resembling in situ degradation, the turnover times are long (slow rates), while the rates are in general faster for studies in which the liquid phase is well-mixed (Tang et al. 2005). It is evident from the literature that using reactors for the bioremediation of PAHs in a soil matrix supports effective degradation rates by counteracting the consequence of mass transfer and thus facilitating an increase in bioavailability by using optimized conditions.
123
360
Strategies to enhance bioremediation efciency For bioremediation to be effective, the overall rate of PAH removal and degradation must be accelerated above naturally occurring microbial processes and the key factor inuencing the bioremediation rate is the bioavailability of the PAHs to the microorganisms (Johnsen et al. 2005; Tang et al. 2005). The literature has documented various strategies, such as the addition of rhizobacteria associated with phytoremediation (rhizoremediation), bacterial chemotaxis, chemical pre-treatment followed by bioremediation, co-metabolism, multiple process integration, bioaugmentation, biostimulation, adaptation, enzyme
mediated remediation and addition of surfactants to enhance and/or improve the degradation rate of the PAHs from contaminated soils (Table 3). Rhizoremediation Although using plants for remediation of persistent contaminants may have advantages over other methods, many limitations exist for large-scale application, including that contaminant sensitivity may retard the establishment of sufcient biomass to facilitate degradation (Huang et al. 2001; Suthersan 2002). Another main potential obstacle that needs to be overcome to improve the phytoremediation system is to increase the low bioavailability
Table 3 Strategies used to enhance the bioremediation of PAH in contaminated soils Strategy Advantages Limitations Large land requirement Reference Huang et al. (2004); Johnson et al. (2004 and 2005); Rentz et al. (2005); Kaimi et al. (2006) Garon et al. (2004); Trindade et al. (2005); Xu (2005a, b); Gong et al. (2005); Betancur-Galvis et al. (2006); Taylor and Jones (2001); Bento et al. (2005); Sabate et al. (2006); Wrenn et al. (2006)
Rhizoremediation Low capital and operating associated cost phytoremediation Effective Biostimulation Low capital cost Can be used in in situ or ex situ remediation process
Effective Bioaugmentation Can be used in ex situ or in situ remediation process Effective and rapid Can be used in ex situ or in situ remediation process Effective and rapid
Other process integration with bioremediation
Adaptation
Addition of surfactants
Can be used in in situ or ex situ remediation process Cheaper and simple technology Low capital and operating cost Enhances bioavalibility Relatively costly process Can be used in in situ or ex situ remediation process
Zheng and Obbard (2002); Garon et al. (2004); Venkata Mohan et al. (2006); Huang et al. (2004); Bento et al. (2005); Trindade et al. (2005) Relatively costly Canet et al. (2001); Lee et al. (2001); Koran process et al. (2001); Goi and Trapido et al. (2004); Huang et al. (2004 (multiple process High maintenance integration); Choi et al. (2001); Johnson cost et al. (2005); Ahn et al. (2005); OMahay et al. (2006); Kulik et al. (2006); Biswas et al. (2005) Relatively Slow Bento et al. (2005); Macleod process and Semple (2005)
Relatively costly compared to natural attenuation process Large land requirement Unpredictable
Bacterial chemotaxins
Cheaper technology and low capital cost Can be used in in situ remediation process
Unpredictable
Kim et al. (2001a, b); Johnsen et al. (2004); Garon et al. (2004); Kumada et al. (2005); Bordas et al. (2005); Zhao et al. (2005); Sartoros et al. (2005); Ohkuma et al. (2006) Ortega-Calvo et al. (2003)
123
361
of pollutants due to adsorption to soil particles (Johnsen et al. 2002). These problems can be efciently counteracted by facilitating phytoremediation through judicious use of both plant growth promoting rhizobacteria and specic contaminantdegrading bacteria. It is known that plants support microora growth in the rhizosphere with much greater adaptability for different carbon sources (including pollutants) (Siciliano and Germida 1998). There is evidence that microbial activity in the rhizosphere or addition of microbial strains to the rhizosphere resulted in enhanced degradation of PAHs by carefully managing the complex plant microbepollutant interactions (Reilley et al. 1996; Joner et al. 2001; Johnson et al. 2004 and 2005; Huang et al. 2004). Rhizobia play an important role in the mixed cropping system (where two or more types of plants are utilized), due to their ability to alleviate nutrient limitations and thus increase plant and root growth by increasing exudation from host roots which in turn facilitates the growth of microbial degraders or inuences pollutant availability (Phillips and Streit 1996; Damaj and Ahmad 1996). Joner et al. (2006) examined the role of mycorrhiza during the remediation of PAHs in a mixed sward of clover and ryegrass and found enhanced loss of chrysene and dibenz[a,h]anthracene in a planted soil containing a mycorrhizal inoculum. Johnson and co-workers (2004) also reported improved remediation of chrysene spiked soil by employing mixed grasslegume systems, together with microbial inoculants (symbiotic rhizobia) and they attributed this to the symbiotic association which improved plant vigor and growth thereby stimulating the rhizospheric microora to degrade chrysene. Johnson et al. 2005 studied a phytoremediation system that consisted of a mixed ryegrass (Lolium perenne) and white clover (Trifolium repens) sward together with a rhizobial inoculum (Rhizobium leguminosarum) for the remediation of PAH-contaminated soil and reported enhanced PAH degradation in planted treatments that received a rhizobial inoculum. The release of 3- and 4-ring PAHs from soil was unaffected by phytoremediation but desorption of 5and 6- ring constituents was increased by two orders of magnitude. Ryegrass growth showed the dissipation threshold of diesel oil contaminated
soil by 55% compared to corresponding root-free soil and the threshold reduction occurred after the development of plant roots (Kaimi et al. 2006). In the rhizosphere, the number of aerobic bacteria and the amount of soil dehydrogenase activity were higher than in the root-free soil and also showed a correlation with the growth of roots. The dissipation rate of diesel oil showed a correlation with soil dehydrogenase activity in both the rhizosphere and the root-free soil. Bioaugmentation Irrespective of rhizobacterial addition in the phytoremediation process, one way of tackling low biomass availability and a lack of required contaminant degraders during bioremediation is to apply a bioaugmentation strategy. In the cases where natural communities of degrading bacteria are present in low numbers or even absent, bioaugmentation, i.e., the addition of contaminant-degrading organisms, may speed up the degradation process (Van Limbergen et al. 1998). Catabolic pathways operating in natural communities reect interactions between microbial species under mixed culture conditions where extensive sharing of nutritional resources is common and interaction of two or several strains is often a pre-requisite for growth and biodegradation (Heinaru et al. 2005). Bioavailability of pollutants and survival and catabolic activity of introduced microorganisms play important roles in bioaugmentation (Heinaru et al. 2005). Several studies have documented the application of a bioaugmentation strategy for PAH degradation in soil by augmenting with specic isolates of bacteria or fungus (Zheng and Obbard 2002; Garon et al. 2004; Trindade et al. 2005; Heinaru et al. 2005; Venkata Mohan et al. 2004b). Garon et al. (2004), reported enhanced degradation of uorene in a soil slurry system by augmenting with a fungi isolate (A. Cylindrospora). In a fungi-augmented system, more than 90% of the uorene was found to be removed within 288 h of contact time, while a non-fungal system required 576 h of contact time. Bioaugmentation is believed to not only augment metabolic function but also inuence the bioavailability of pollutants. This, when the
123
362
application methods involve homogenization, slurrying, or intensive ushing of the system, or when the bacteria added, differ from the indigenous population with respect to their specic afnity for the contaminant, maintenance requirements, ability to co-utilize natural substrates, active or passive mobility, adhesion behavior, or ability to produce biosurfactants and to ingest surfactant solubilized chemicals (Johnsen et al. 2005). Adaptation Adaptation is another strategy or process which facilitates increases in the oxidizing potential of the native community (Spain et al. 1980). Recent studies by Macleod and Semple (2002), Reid et al. (2002) and Lee et al. (2003) have shown the positive role of adaptation on bioremediation efciency. Adaptation can occur either through the induction and/or depression of specic enzymes or by the development of new metabolic capabilities through genetic changes or by the selective enrichment of organisms able to transform the target contaminant (Spain et al. 1980; Leahy and Colwell 1990). It is evident that the longer the contaminant is in the soil, the greater is the level of the catabolic activity. It has been suggested that pre-exposure of soils to concentrations greater than background are needed for adaptation to a contaminant (Spain and Van Veld 1983). Macleod and Semple (2005) demonstrated considerable improvement in the derivative abilities of a soil microbial community over a range of pyrene concentrations and applications. Adaptation was shown through the development of the catabolic activity of pyrene-degrading bacteria in the soil. Bouchez et al. (1999) showed that augmenting with mixed cultures of two or three strains, although possessing the capacity to mineralize each of ve PAHs, achieved limited degradation of a ve-PAH mixture. In contrast, an enrichment from a PAH-contaminated soil readily mineralized the ve-PAH mixture. Co-metabolism Under soil conditions, bacteria may not utilize a single carbon source, but rather co-utilize a
number of available carbon compounds (Egli 2002). Co-metabolism can be dened as a nonspecic enzymatic reaction, with a substrate competing with the structurally similar primary substrate for the enzymes active site. The formation of enzymes catalyzing the degradation of organic pollutants may be repressed when the cells grows on other substrates, but the constitutive background level of expression is often sufcient for immediate consumption of the pollutant if it becomes available in low amounts (Egli 2002). Several studies have shown that the presence of co-substrates enhanced PAH degradation (Kanaly et al. 1997; Kanaly and Bartha 1999; Yuan et al. 2000; Taylor and Jones 2001; Chang et al. 2002; Garon et al. 2004; Ambrosoli et al. 2005; Gong et al. 2005). Chang et al. (2002) have shown analogous results in their anaerobic experiments, where different carbon sources enhanced PAH degradation due to the growth of methanogens, thus leading to an increased rate of degradation. Enhanced PAH degradation in the presence of acetate might be attributed to the effect of co-metabolic fermentation activities by the inoculum, which helps to utilize PAHs not only as electron donors, but also as acceptors (Ambrosoli et al. 2005). By supplementing soil slurry systems with maltosyl-cyclodextrin (branched cyclodextrin) enhanced bioavailability of uorene resulting in effective degradation was shown (Garon et al. 2004). As a consequence, if the cells concomitantly take up several carbon sources to maintain their biomass, there will not necessarily be a threshold concentration of PAH, below which biodegradation stops (Boonchan et al. 2000; Johnsen et al. 2005). Biostimulation Biostimulation is one important strategy which has been used extensively for enhancing the bioremediation of PAHs in soil (Gijs and Sparrevik 2000; Taylor and Jones 2001; Chang et al. 2002; Delille et al. 2004; Garon et al. 2004; BetancurGalvis et al. 2006, Coulon et al. 2005; Gong et al. 2005; Sabate et al. 2006; Trindade et al. 2005; Xu et al. 2005a, b). It involves adjustments to the site by the addition of nutrients (nitrogen, phosphorus and trace minerals) while also making appropriate
123
363
pH adjustments, soil moisture content, and aeration for the proliferation of indigenous microorganisms in order to provide bacterial communities with a favorable environment by which they can effectively degrade contaminants (Salanitro et al. 1997). Biostimulation agents are commonly used to overcome limitations in microbial growth and activity. Stimulation with the addition of fertilizers has been shown to increase the number and activity of microbial populations, thus enhancing degradation in soils (Breedveld and Sparrevik 2000; Betancur-Galvis et al. 2006; Xu and Obbard 2003). However, relatively little attention has been given to the effects of macronutrients on the biodegradation of PAHs (Betancur-Galvis et al. 2006). Tang et al. (2005) pointed out that the biodegradation rate was enhanced only by the addition of nitrate and phosphate in sites when the background nutrients are insufcient. In addition to supplementing with nutrients, addition of agents such as bio-diesel (Taylor and Jones 2001), municipal sewage (Chang et al. 2002), oil renery sludge (Chang et al. 2002), biosolids (Betancur-Galvis et al. 2006), sunower oil (Gong et al. 2005) and chitosan (Xu et al. 2005a, b) as potential co-substrates has been tried. By facilitating aeration and adjusting soil water content (Sabate et al. 2006) these potential co-substrates showed positive inuence on bioremediation rates. Temperature plays a signicant role in controlling the nature and extent of microbial hydrocarbon metabolism (Nedwell 1999), the physical nature and chemical composition of hydrocarbons (Whyte et al. 1998; Rowland et al. 2000) and the bioavailability of soluble hydrophobic substances (Coulon et al. 2005). Increases in temperature lead to increases in diffusion rates of organic compounds by a decrease in their viscosity which lead to increases in the bioavailability of hydrophobic pollutants by increasing solubility, diffusion and reaction rates (Northcott and Jones 2001). Indeed, higher molecular reaction rates due to smaller boundary layers are expected at elevated temperatures. Feitkenhauer et al. (2003) showed that a mixture of 3- to 5- ring PAHs were degraded at 65C by a mixed culture when hexadecane was included as a degradable solvent. In contrary, the increased volatilization
and solubility of some hydrocarbons at elevated temperature may enhance their toxicity (Whyte et al. 1998; Niehaus et al. 1999) and such an increase in toxicity may delay the onset of degradation (Leahy and Colwell 1990; Itavaara et al. 2000). Although microbial activity is generally reduced at low temperatures, many of the components in crude oil and diesel were reported to be degraded by psychrophilic and psychrotrophic microorganisms (Delille and Delille 2000; Gibb et al. 2001; Baraniecki et al. 2002; Eckford et al. 2002; Eriksson et al. 2001). Field tests revealed that soil coverage with plastic sheets induced a small but permanent increase in the temperature of the surface soil and favored the degradation of alkanes over aromatics (Delille et al. 2004). However, the use of biopile systems seems to be the most economic way to reach large increases in temperature (Delille et al. 2004). Careful evaluation of the temperature effects on biodegradation rates in laboratory scale experiments may give more insight into the process before going to applications in the eld. Surfactant addition It is evident that PAH bioavailability is limited by low solubility and strong sorption/sequestration in micropores or organic matter, non-uniform spatial distribution of microorganisms and pollutants, and the retardation of substrate diffusion by the soil matrix (Harms and Bosma 1997; Chung and Alexander 1999; Johnsen et al. 2005; Tang et al. 2005). When mass transfer is the limiting factor, homogenization and dispersion of the contaminants may enhance the biodegradation rates. A way to disperse pollutants is by the addition of surface active compounds such as surfactants, which facilitate or improve pollutant transfer into the water phase by decreasing the interfacial tension between water and hydrophobic pollutants. Addition of surfactant can improve PAH transport to the degraders by inuencing the dissolution or desorption process by attaching to the PAH-water interface (Park et al. 2000; Kim et al. 2001a, b; Bordes et al. 2005; Johnsen et al. 2005; Tang et al. 2005; Zhao et al. 2005). Zhao et al. (2005) showed the positive effect of mixed anionicnonionic surfactants on the remediation
123
364
of PAH contaminated soils and the degree of solubility enhancements by the mixed surfactants followed the order of SDSTW80 > SDS Brij35 > SDSTX100. On contrary, Garcia et al. (2001) showed the reduced bioavailability of sorbed contaminants after addition of surfactant due to the rate-limiting intraparticle diffusion of contaminants that remained uninuenced by the surfactant and the reduction of the water-dissolved contaminant concentration by solubilization into micelles. Another way to biologically increase the effective diffusion of PAH molecules would be the excretion of biosurfactants as carriers (Garcia et al. 2001; Johnsen et al. 2004) where the micelles of the surfactant facilitate the diffusive transfer of contaminant through the boundary layer. Biosurfactants are small, detergent-like molecules with a hydrophilic head and a lipophilic tail which form spherical or lamellar micelles when the surfactant concentration exceeds a compound-specic, critical micelle concentration (Johnsen et al. 2005). Hydrophobic compounds become solubilized in the hydrophobic cores of the micelles, which lead to a transfer of PAH from solid, liquid, or sorbed PAH-pools into the water phase. Villemur et al. (2000), studied the inuence of addition of silicone oil in soil slurry systems to promote desorption of PAHs from soil to increase their bioavailability. The addition of water immiscible, non-biodegradable and biocompatible silicon oil showed enhanced efciency over the corresponding control system without the oil. Chemical pre-treatment PAHs are stable compounds, and the initial oxidation step is biologically slow and metabolically expensive (Alexander 1999; Huang et al. 2001). Chemical methods offer a relatively rapid and aggressive alternative to overcome some of the problems associated with bioremediation and such methods are not sensitive to the type and concentration of contaminant (Kim and Choi 2002). Integration of chemical treatment prior to bioremediation was reported to be an efcient strategy to enhance the degradation rates of PAH-contaminated soil. Integration of solvent pre-treatment (Koran et al. 2001; Lee et al. 2001)
and chemical oxidation (Choi et al. 2001; Goi and Trapido 2004; Kulik et al. 2006; Ahn et al. 2005; OMahony et al. 2006) prior to bioremediation was reported (Table 1). More stress was observed in the application of ozone oxidation alone (Choi et al. 2001; Goi and Trapido et al. 2004; Ahn et al. 2005; OMahony et al. 2006) or in the combination with Fentons treatment (Kulik et al. 2006) with different degrees of success. The important merits of ozone include that it can be used either in gaseous or liquid form and after a short period of application the un-reacted ozone reverts back to atmospheric oxygen without leaving toxic residues in the soil (KasprzykHordern et al. 2003; Kulik et al. 2006). Moreover, ozone transforms PAHs into intermediates that are more soluble in the aqueous phase and therefore more available to microbes for biodegradation. Combined chemical and biological treatment for PAH-contaminated soils has been investigated (OMahony et al. 2006; Kulik et al. 2006). Kulik et al. (2006) studied the ability of pre-oxidation using ozonation and Fenton-like treatment to overcome PAH recalcitrance to biodegradation and concluded that combined chemical and biological treatment was more efcient in PAH elimination in creosote-contaminated soil than in either one alone. Ahn et al. (2005) investigated the PAH degradative potential of indigenous microorganisms in ozonated soil. pH and microbial concentrations in the soils were found to decrease with increases in ozonation time and the greatest reduction was observed in soil that was ozonated for 900 min. However, highest removal after bioremediation was observed in 180 min-ozonated soil while a negligible removal was shown in 900 min-ozonated soil. They concluded that appropriate ozonation time combined with the activity of the indigenous microorganisms that survived after ozonation could enhance remediation. OMahony et al. (2006) studied the potential of using ozone treatment with bioremediation for the removal of phenanthrene from different types of soils. Moisture content of the soil and the presence of clay showed signicant inuence on the degradation efciency. Comparatively air-dried soils showed the greatest removal of phenanthrene and presence of clay showed retarded treatment
123
365
efciency. They concluded that pre-ozonation did not enhance the subsequent biodegradation of phenanthrene in the soils and this was attributed to the release of toxic by-products in this soil during ozonation. Application of adsorption as pre-treatment to bioremediation (Biswas et al. 2005), multiple process integration, such as physical, photochemical, bioremediation and phytoremediation (Huang et al. 2004), and combined treatment with rye grass and rhizobacterium (Johnson et al. 2005) were also reported to be effective. Koran et al. (2001) studied the integration of soil solvent washing prior to anaerobic treatment in a uidized bed reactor with GAC as biomass supporting material with a good degree of success. Biswas et al. (2005) elucidated the role of adsorbents such as peat-sorb and spill-sorb in adsorbing diesel oil-contaminated soil by integration with soil slurry phase bioremediation. It is evident from the literature that integrating chemical treatment prior to biological treatment is encouraging, however appropriate precautions should be taken to optimize the conditions such that effective chemical treatment will result without inhibiting the native soil microora. Anaerobic and anoxic microenvironment Strategies involving microenvironment/metabolic function in bioremediation processes signicantly inuence the degradation rates and efciency of degradation of PAHs. Compared to aerobic metabolic function, the anaerobic microenvironment (Koran et al. 2001; Chang et al. 2002; Boopathy 2003 and 2004; Ambrosoli et al. 2005; Kuwono and Shimizu 2006) has been relatively less investigated in the case of soil bound PAH bioremediation. In more recent times, application of anaerobic process for the degradation of PAHcontaminated soils has been documented (Kanaly and Harayama, 2000; Meckenstock et al. 2000; Samanta et al. 2002; Johnsen et al. 2005). In the soil environment, anaerobic biodegradation of PAHs is possible both through fermentative and respiratory metabolism, provided that suitable terminal electron acceptors (nitrate, sulfate, or ferric iron) are present (Meckenstock et al. 2000; Ambrosoli et al. 2005). Chang et al. (2002) investigated the anaerobic degradation of PAHs
in different types of soils under nutrient enrichment conditions and their research indicated that rapid individual PAH degradation rates were observed in a mixture of PAH substrates compared to the presence of a single substrate. Anaerobic degradation of 2-, 3-, and 4ring PAHs was observed at optimal incubation conditions of pH 8.0 and 30C. Among the three anaerobic conditions studied, sulfate- reducing conditions (SRC) showed the highest efciency compared to methanogenic conditions and nitrate-reducing conditions (NRC). Boopathy (2003 and 2004) used anaerobic environments in soil slurry phase systems under mixed electron acceptor conditions with a good degree of success for the bioremediation of diesel fuel sediments. Extensive research is being conducted in the laboratories of Dr. Y. Shimizu, Kyoto University, on the remediation of coal-derived hydrocarbon contaminated soil under both aerobic and anaerobic conditions employing soil column bioreactors. Kuwano and Shimizu (2006) reported bioremediation of coal-derived hydrocarbon contaminated soil under SRC in soil column bioreactors. The experimental data revealed the effectiveness of SRC in transforming higher molecular weight PAHs to low molecular weight PAHs and suggested that the integration of aerobic processes after anaerobic operations would result in further remediation of low molecular weight PAHs. Koran et al. (2001) developed an integrated system to remediate soils contaminated with pentachlorophenol and PAHs by the coupling of two treatment technologies, soil-solvent washing and anaerobic biotreatment (uidized bed) of the extract. The reactor achieved a removal efciency of approximately 86% (naphthalene) and 93% (acenaphthene). However, anoxic conditions which normally exist in the soil environment have not so far been studied in the remediation of PAHs. The potential advent of anoxic microenvironment engineering capabilties with the arrival of sequencing batch reactors (SBR) may provide effective microenvironments for transforming soil bound PAHs. Cassidy and Irvine (1997) showed the potential advantage of SBR operation in the degradation of diesel fuelcontaminated soil compared to continuous mode operation. The SBR process operation, otherwise
123
366
called periodic discontinuous operation, may have potential to inuence the microbial system by enforcement of controlled short-term unsteady state conditions leading in the long run to stable steady state conditions, with respect to the composition and metabolic properties of the microbial population by controlling the distribution and physiological state of the microorganisms (Wilderer et al. 2001). SBR systems have high substrate uptake capability due to the alternation between high carbon source and starvation conditions and the systems are generally more robust to withstand the shock loads (Wilderer et al. 2001). The application of SBR operation to PAH bioremediation may have the advantage of providing an anoxic microenvironment integrated with an aerobic microenvironment in single reactor system (Venkata Mohan et al. 2004a and 2006) and also have the advantage of integrating two metabolic functions. Enzyme-mediated bioremediation The catalytic action of enzymes is extremely efcient and selective compared to chemical catalysts due to higher reaction rates, milder reaction conditions, greater stereospecicity and the capability to catalyze reactions at relatively low temperature and in the entire pH range (Venkata Mohan et al. 2002). Application of enzyme biocatalyst treatment in the remediation of PAHcontaminated soil is recently nding its place (Table 1). Zheng and Obbard (2002, 2003) used white rot fungus (Phanerochaete chrysosporium) synergistically, in conjugation with soil indigenous microorganisms in the oxidation of PAHs. They observed an enhanced oxidation by 43% in the presence of fungus while limited oxidation occurred for high molecular weight PAHs (chrysene, benzo[a]pyrene, dibenz[a,h]anthracene and benzo[g,h,i]perylene). Laccase from Pleurotus ostreatus1804 was studied to evaluate its potential to oxidize anthracene-contaminated soil in a sole-substrate system in the presence of 2,2azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) as mediator (Venkata Mohan et al. 2004b). Results showed enzymatic transformation of anthracene in the soil matrix to a less toxic intermediate (anthraquinone) indicating the
applicability of fungus oxidation. Laccases and phenoloxidases catalyze the oxidation of PAHs in the presence of mediator compounds that act as electron shuttles between the free enzyme and the substrate. Garon et al. (2004) studied the applicability of fungus (Absidia cylindrospora) as a bioaugmentation supplement in soil slurry systems to enhance uorene bioremediation in contaminated soil. Fungi biocatalyst systems, which are relatively less studied, may have signicant advantages over bacterial systems for soil bioremediation and in particular for PAH transformation. Fungi are generally found in aquatic sediments, terrestrial habitats and surface waters and they have specic advantages over bacteria where fungal hyphal growth may penetrate throughout the contaminated soil to reach PAHs (Aprill and Sims 1990). Moreover, fungi have extracellular enzymes involved in the degradation of a wide range of pollutants (Garon et al. 2004). Bacterial chemotaxis Recently, considerable interest is occurring in regard to the application of bacterial chemotaxis as potential tool to enhance bioremediation. Chemotaxis is dened as the phenomena of bacterial movement under the inuence of a chemical gradient, either toward (positive chemotaxis) or away (negative chemotaxis) from the gradient which helps bacteria to nd optimum conditions for their growth and survival (Pandey and Jain 2002). It is a complex process in which bacterial cells detect temporal changes in the concentration of specic chemicals, respond behaviorally to these changes and then adapt to the new concentration of the chemical stimuli (Samanta et al. 2002). Through evolution, microorganisms have developed effective mechanisms that help them to regulate their cellular function in response to changes in their environment (Hoch 2000). Chemotaxis can increase an organisms chances of locating useful sources of carbon, nitrogen and energy, and could thus play an important role in the biodegradation process (Parales and Harwood 2002). Several studies showed evidence that motile bacteria are chemotactically attracted to environmental pollutants that they subsequently degraded. In conjunction with their biodegrada-
123
367
tive capacities, bacterial chemotaxis towards pollutants might contribute to the ability of bacteria to compete with other organisms in the environment and to be efcient agents for bioremediation (Parales and Haddock 2004). Indeed, coordinated regulation of bacterial chemotaxis toward almost all toxic compounds and their respective mineralization and/or transformation indicate that this phenomenon might be an integral feature of degradation (Pandey and Jain 2002). Recently, research addressing the possibility of a role for chemotaxis in the biodegradation of PAHs was documented (Ortega-Calvo et al. 2003; Parales and Haddock 2004). OrtegaCalvo and co-workers (2003) for the rst time evaluated chemotaxis as a bioavailability-promoting trait in PAH-degrading bacteria from the soil rhizosphere. Out of 20 motile strains capable of degrading different PAHs, 3 representative Pseudomonas strains were used for chemotaxis studies with PAHs (naphthalene, phenanthrene, anthracene, and pyrene) along with bacterial lipopolysaccharide and root exudates. The results indicated that chemotaxis is a relevant mobilizing factor for PAH-degrading rhizosphere bacteria. Because the chemotaxis of bacteria seems to aid in the degradation of toxic compounds, the molecular basis of this phenomenon is a fertile and useful area for future research, particularly in regard to soil contaminated with PAHs. Biomimetic catalysis In the soil environment, humic substances play important roles in the remedial process via a variety of interactions, including solubilization and electron transfer (Fukushima et al. 2003). Humic substances are heterogeneous polyelectrolytes, which contain a variety of functional groups and structural moieties and the chemical characteristics vary by soil type (Gaffney et al. 1996). In radical-based oxidative reactions (e.g., enzymatic, Fenton, and MnO2 oxidations), the removal of organic pollutants may be enhanced or inhibited in the presence of humic substances (Morimoto and Tatsumi 1997; Fukushima and Tatsumi 2001; Fukushima et al. 2003). Such enhancement was attributed to the coupling of radical species from organic pollutants with humic substances and in
contrast, inhibition was attributed to humic substances serving as scavengers of active oxygen species, which may have acted as strong oxidants to organic pollutants (Klausen et al. 1997). Thus, humic substances also inuence the removal of organic pollutants via biomimetic catalytic systems (Fukushima et al. 2003). Taking advantage of this phenomenon, biomimetic catalytic systems were investigated recently for remediation of soilbound contaminants by mimicking the transformations of xenobiotics (Marimoto and Tatsumi 1997; Fukushima and Tatsumi 2001; Fukushima et al. 2003). Due to its specic advantages, especially in humic soils, the biomimetic catalytic systems may also be evaluated for the remediation of PAH-contaminated soil. Multiple process integration One of the major challenges for organisms to degrade intact PAHs is the initial oxidation step. Due to the presence of p-orbital structures in intact PAHs, a large thermodynamic barrier to the initial biological oxidation step is created (Huang et al. 2001). In such cases photochemical pretreatment of contaminated soil may facilitate the bioremediation of PAHs because they can be readily photooxidized by sunlight to quinones and hydroxy quinones (Mallakin et al. 2000). When land farming was carried out prior to phytoremediation so that a new layer of soil was exposed to sunlight, the PAHs brought to the surface were photooxidized (Huang et al. 2004). Land farming may also oxygenate the soil, potentially improving the growth of aerobic soil bacteria, thereby resulting in faster degradation of contaminants. In this direction, Huang and co workers (2004) developed a multiple process technique, integrating a phytoremediation system composed of physical (volatilization), photochemical (photooxidation), microbial remediation and phytoremediation for the remediation of creosote-contaminated soil. The applied techniques were land-farming (aeration and light exposure), introduction of contaminant degrading bacteria, plant growth promoting rhizobacteria and plant growth of a contaminant-tolerant tall fescue (Festuca arundinacea). Over a 4-month period, the average efciency of removal of 16
123
368
Rev Environ Sci Biotechnol (2006) 5:347374 Alexander M (1999) Biodegradation and bioremediation. Academic Press, San Diego Alexander M (2000) How toxic are toxic chemicals in soil? Enviro Sci Technol 34: 42594265 Ambrosoli R, Petruzzelli L, Minati JL, Marsan FA (2005) Anaerobic PAH degradation in soil by a mixed bacterial consortium under denitrifying conditions. Chemosphere 60:12311236 Antizar-Ladislao A, Lopez-Real JM, Beck AJ (2004) Bioremediation of polycyclic aromatic hydrocarbon (PAH)-contaminated waste using composting approaches. Crit Rev Environ Sci Technol 34:249289 Antizar-Ladislao B, Lopez-Real J, Beck AJ (2005a) Invessel composting bioremediation of aged coal tar soil: effect of temperature and soil/green waste amendment ratio. Environ Int 31:173178 Antizar-Ladislao B, Lopez-Real J, Beck AJ (2005b) Laboratory studies of the remediation of polycyclic aromatic hydrocarbon contaminated soil by in-vessel composting. Waste Manag 25:281289 Antizar-Ladislao B, Lopez-Real J, Beck AJ (2006) Degradation of polycyclic aromatic hydrocarbons (PAHs) in an aged coal tar contaminated soil under in-vessel composting conditions. Environ Pollut 141:459468 Aprill W, Sims RC (1990) Evaluation of the use of prairie grasses for stimulating polycyclic aromatic hydrocarbon treatment in soil. Chemosphere 20:253265 Baptista SJ, Cammarota MC, Freire DDC (2005) Production of CO2 in crude oil bioremediation in clay soil. Braz Arch Biol Technol 48:249255 Baraniecki C, Aislabie J, Foght J (2002) Characterization of Sphingomonas sp. Ant 17, an aromatic hydrocarbon-degrading bacterium isolated from Antarctic soil. Microb Ecol 43:4454 Bento FM, Camargo FAO, Okeke BC, Frankenberger WT (2005) Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresource Technol 96:10491055 Betancur-Galvis LA, Alvarez-Bernal D, Ramos-Valdivia AC, Dendooven L (2006) Bioremediation of polycyclic aromatic hydrocarbon-contaminated salinealkaline soils of the former Lake Texcoco. Chemosphere 62:17491760 Biswas SSK, Chaudhari S, Mukherji S (2005) Microbial uptake of diesel oil sorbed on soil and oil spill clean-up sorbents. J Chem Technol Biotechnol 80:587593 Bogan BW, Sullivan WR, Cruz KH, Paterek JR, Ravikovitch PI, Neimark AV (2003) Humic coverage index as a determining factor governing strain-specic hydrocarbon availability to contaminant degrading bacteria in soils. Environ Sci Technol 37:51685174 Bollag JM (1992) Decontaminating soil with enzymes. Environ Sci Technol 26:18761881 Boonchan S, Britz ML, Stanley GL (2000) Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by dened fungalbacterial cocultures. Appl Environ Microbiol 66:10071019 Boopathy R (2003) Anaerobic degradation of No. 2 diesel fuel in the wetland sediments of Barataria-Terrebonne
priority PAHs by this multi-process remediation system was twice that of land-farming, 50% more than bioremediation alone and 45% more than phytoremediation by itself. Conclusions Considering that bioremediation technology has proven to be effective, economic and eco-friendly for the treatment of PAH-contaminated soils, focused research in some specic areas is desired for more effective treatment design and performance. Some areas where further research may be directed include strategies to enhance bioavailability and mass transfer of contaminants, optimization of process factors and system congurations, and multiple process integration. The potential advantage of anaerobic metabolic functions in degrading the higher molecular weight PAHs is well established at the single species level under different electron acceptor conditions; however its application has been relatively less investigated for soil-bound PAH bioremediation in mixed microbial systems. The potentiality of anaerobic metabolic function alone or integrated with aerobic metabolic function may still be investigated. The role of the anoxic microenvironment on PAH transformation in the soil matrix is also an area where not much work has yet been documented. With the advent of periodic discontinuous process operations and its associated advantages in wastewater treatment processes, these process operations may be benecially extended to include PAH bioremediation if appropriate system design and optimization are implemented. Fungal-catalyzed processes for enhanced transformation of PAHs is also an area where further research may be pursued. Lastly, research on the application of biomimetic catalytic systems and bacterial chemotaxis should be continued, especially for PAH bioremediation in the soil matrix. References
Ahn Y, Jung H, Tatavarty R, Choi H, Yang J, Kim IS (2005) Monitoring of petroleum hydrocarbon degradative potential of indigenous microorganisms in ozonated soil. Biodegradation 16:4556
123
Rev Environ Sci Biotechnol (2006) 5:347374 estuary under various electron acceptor conditions. Bioresource Technol 86:171175 Boopathy R (2004) Anaerobic biodegradation of No. 2 diesel fuel in soil: a soil column study. Bioresource Technol 94:143151 Bordas F, Lafrance P, Villemur R (2005) Conditions for effective removal of pyrene from an articially contaminated soil using Pseudomonas aeruginosa 57SJ rhamnolipids. Environ Pollut 138:6976 Bosma TNP, Middeldorp PJM, Schraa G, Zehnder AJB (1997) Mass transfer limitation of biotransformation: quantifying bioavailability. Environ Sci Technol 31:248252 Bouchez M, Blanchet D, Bardin V, Haeseler F, Vandecasteele JP (1999) Efciency of dened strains and of soil consortia in the biodegradation of polycyclic aromatic hydrocarbon (PAH) mixtures. Biodegradation 10:429435 Breedveld GD, Sparrevik M (2000) Nutrient-limited biodegradation of PAH in various soil strata at a creosote contaminated site. Biodegradation 11:391399 Canet R, Birnstingl JG, Malcolm DG, Lopez-Real JM, Beck AJ (2001) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by native microora and combinations of white-rot fungi in a coal-tar contaminated soil. Bioresource Technol 76:113117 Cassidy DP, Irvine RL (1997) Biological treatment of a soil contaminated with diesel fuel using periodically operated slurry and solid phase reactors. Water Sci Technol 35:185192 Cerniglia CE (1984) Microbial metabolism of polycyclic aromatic hydrocarbons. Adv Appl Microbiol 30:3171 Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351368 Chang BV, Shiung LC, Yuan SY (2002) Anaerobic biodegradation of polycyclic aromatic hydrocarbon in soil. Chemosphere 48:717724 Choi H, Kim YY, Lim H, Cho J, Kang JW, Kim KS (2001) Oxidation of polycyclic aromatic hydrocarbons by ozone in the presence of sand. Water Sci Technol 43:349356 Chung N, Alexander M (1999) Effect of concentration on sequestration and bioavailability of two polycyclic aromatic hydrocarbon. Environ Sci Technol 33:36053608 Coulon F, Pelletier E, Gourhant L, Delille D (2005) Effects of nutrient and temperature on degradation of petroleum hydrocarbons in contaminated subAntarctic soil. Chemosphere 58:14391448 Cunningham CJ, Ivshina IB, Lozinsky VI, Kuyukina MS, Philp JC (2004) Bioremediation of diesel-contaminated soil by microorganisms immobilised in polyvinyl alcohol. Int Biodeter Biodegradation 54:167 174 Cuypers A, Vangronsveld J, Clijsters H (2002) Peroxidases in roots and primary leaves of Phaseolus vulgaris: copper and zinc phytotoxicity: a comparison. J Plant Physiol 159:869876 Damaj M, Ahmad D (1996) Biodegradation of polychlorinated biphenyls by rhizobia: a novel nding. Biochem Biophys Res Commun 218:908915
369 Davis JW, Madsen S (1996) Factors affecting the biodegradation of toluene in soil. Chemosphere 33:107130 Delille D, Delille B (2000) Field observations on the variability of crude oil impact on indigenous hydrocarbon-degrading bacteria from sub-antarctic intertidal sediments. Mar Environ Res 49:403417 Delille D, Coulon F, Pelletier E (2004) Biostimulation of natural microbial assemblages in oil-amended vegetated and desert sub-Antarctic. Microb Ecol 47:407415 Doick KJ, Semple KT (2003) The effect of soil:water ratios on the mineralisation of phenanthrene: LNAPL mixtures in soil. FEMS Microbiol Lett 220:2933 Eckford RF, Cook DD, Aislabie SJ, Foght J (2002) Freeliving heterotrophic nitrogen-xing bacteria isolated from fuel-contaminated Antarctic soils. Appl Environ Microbiol 68:51815185 Egli T (2002) Microbial degradation of pollutants at low concentrations and in the presence of alternative carbon substrates: emerging patterns. In: Agathos SN, Reineke W (eds) Focus on biotechnology. Biotechnology for the environment: strategy and fundamentals, vol 3A. Kluwer Academic Publishers, Dordrecht, pp 131139 Ehlers LJ, Luthy RG (2003) Contaminant bioavailability in soil and sediment. Environ Sci Technol 37:295A 302A Eriksson M, Ka JP, Mohn WW (2001) Effects of low temperature and freezethaw cycles on hydrocarbon biodegradation in Arctic tundra soil. Appl Environ Microbiol 67:51075112 Eweis BJ, Ergas JS, Chang PYD, Schroeder DE (1998) Bioremediation principles. WCB McGraw-Hill, Malaysia Fava F, Berselli S, Conte P, Piccolo A, Marchetti L (2004) Effects of humic substances and soya lecithin on the aerobic bioremediation of a soil historically contaminated by polycyclic aromatic hydrocarbons (PAHs). Biotechnol Bioeng 88:214223 Feitkenhauer H, Muller R, Markl H (2003) Degradation of polycyclic aromatic hydrocarbons and long chain alkanes at 6070C by Thermus and Bacillus spp. Biodegradation 14:367372 Ferro AM, Sims RC, Bugbee B (1994) Hycrest crested wheatgrass accelerates the degradation of pentachlorophenol in soil. J Environ Qual 23:272279 Fukushima M, Tatsumi K (2001) Degradation pathways of pentachlorophenol by photo-fenton systems in the presence of iron(III), humic acid and hydrogen peroxide. Environ Sci Technol 35:17711778 Fukushima M, Sawada A, Kawasaki M, Ichikawa H, Morimoto K, Tatsumi K, Aoyama M (2003) Inuence of humic substances on the removal of pentachlorophenol by a biomimetic catalytic system with a watersoluble iron(III)porphyrin complex. Environ Sci Technol 37:10311036 Gaffney JS, Marley NA, Clark SB (1996) Humic and fulvic acids: isolation, structure and environmental role. American Chemical Society Symposium Series 651
123
370 Garcia JM, Wick LY, Harms H (2001) Inuence of the nonionic surfactant Brij 35 on the bioavailability of solid and sorbed dibenzofuran. Environ Sci Technol 35:20332039 Garon D, Sage L, Wouessidjewe D, Seigle-Murandi F (2004) Enhanced degradation of uorine in soil slurry by Absidia cylindrospora and maltosyl-cyclodextrin. Chemosphere 56:159166 Gibb A, Chu A, Wong RCK, Goodman RH (2001) Bioremediation kinetics of crude oil at 5C. J Environ Eng 127:818824 Gijs DB, Sparrevik M (2000). Nutrient-limited biodegradation of PAH in various soil strata at a creosote contaminated site. Biodegradation 11:391399 Gogoi BK, Dutta NN, Goswami P, Krishna Mohan TR (2003) A case study of bioremediation of petroleumhydrocarbon contaminated soil at a crude oil spill site. Adv Environ Res 7:767782 Goi A, Trapido M (2004) Degradation of polycyclic aromatic hydrocarbons in soil: the Fenton reagent versus ozonation. Environ Technol 25:155164 Gong Z, Alef K, Wilke B, Mai M, Li P (2005) Assessment of microbial respiratory activity of a manufactured gas plant soil after remediation using sunower oil. J Hazard Mater B124:217223 Guerin TF (1999) Bioremediation of phenols and polycyclic aromatic hydrocarbons in creosote contaminated soil using ex-situ land treatment. J Hazard Mater B65:305315 Guerin TF (2000) Long-term performance of a land treatment facility for the bioremediation of non-volatile oily wastes. Resour Conserv Recycl 28:105120 Guerin WF, Boyd SA (1997) Bioavailability of naphthalene associated with natural and synthetic sorbents. Water Res 31:15041512 Guerin WF, Mueller SA, Boyd SA (1992) Quantitative assessment of sorbed substrate bioavailability using a mineralization kinetics approach. 84th Annual Meeting, Soil Science Society of America Haderlein A, Legros R, Ramsay BA (2005) Pyrene mineralization capacity increases with compost maturity. Biodegradation (in press) Hansen LD, Nestler C, Ringelberg D, Bajpai R (2004) Extended bioremediation of PAH/PCP contaminated soils from the POPILE wood treatment facility. Chemosphere 54:14811493 Harayama S (1997) Polycyclic aromatic hydrocarbon bioremediation design. Curr Opin Biotechnol 8:268 273 Harms H, Bosma TNP (1997) Mass transfer limitation of microbial growth and pollutant degradation. J Ind Microbiol18:97105 Harmsen J (2004) Landfarming of polycyclic aromatic hydrocarbons and mineral oil contaminated sediments. PhD Thesis, Wageningen University, Wageningen Hatzinger PB, Alexander M (1999) Effects of aging chemicals in soil and their biodegradability and extractability. Environ Sci Technol 29:537545 Heinaru E, Merimaa M, Viggor S, Lehiste M, Leito I, Truu J, Heinaru A (2005) Biodegradation efciency of functionally important populations selected for
Rev Environ Sci Biotechnol (2006) 5:347374 bioaugmentation in phenol- and oil-polluted area. FEMS Microb Ecol 51:363373 Hoch JA (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3:165170 Huang X, Alawi YE, Penrose DM, Glick BR, Greenberg BM (2004) A multi-process phytoremediation system for removal of polycyclic aromatic hydrocarbons from contaminated soils. Environ Pollut 130:465476 Huang XD, Glick BR, Greenberg MB (2001) Combining remediation technologies increases kinetics for removal of persistent organic contaminants from soil. In: Greenberg BM (eds) Environmental toxicology and risk assessment. ASTM Johnsen AR, Wickb LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:7184 Johnsen AR, Winding A, Karlson U, Roslev P (2002) Linking of micro-organisms to phenanthrene metabolism in soil by analysis of 13C-labelled cell-lipids. Appl Environ Microbiol 68:61066113 Johnson DL, Maguire KL, Anderson DR, McGrath SP (2004) Enhanced dissipation of chrysene in planted soil: the impact of a rhizobial inoculum. Soil Biol Biochem 3:3338 Johnson DL, Anderson DR, McGrath SP (2005) Soil microbial response during the phytoremediation of a PAH contaminated soil Soil Biology. Biochemistry 37:23342336 Joner EJ, Johansen A, Loibner AP, Cruz MA, Szolar OHJ, Portal JM, Leyval C (2001) Rhizosphere effects on microbial community structure and dissipation and toxicity of polycyclic aromatic hydrocarbons (PAHs) in spiked soil. Environ Sci Technol 35:27732777 Joner EJ, Leyval C, Colpaert JV (2006) Ectomycorrhizas impede phytoremediation of polycyclic aromatic hydrocarbons (PAHs) both within and beyond the rhizosphere. Environ Pollut 142:3438 Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of Benzo[a] pyrene. Int Biodeterior Biodegradation 45:5788 Kaimi E, Mukaidani T, Miyoshi S, Tamaki M (2006) Ryegrass enhancement of biodegradation in dieselcontaminated soil. Environ Exp Botany 55:110119 Kanaly RA, Bartha R, Fogel S, Findlay M (1997) Biodegradation of [14C]benzo[a]pyrene added in crude oil to uncontaminated soil. Appl Environ Microbiol 63:45114515 Kanaly RA, Bartha R (1999) Cometabolic mineralization of benzo[a]pyrene caused by hydrocarbon additions to soil. Environ Toxicol Chem 18:21862190 Kanaly RA, Harayama S (2000) Biodegradation of high molecular weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:20592067 Kasprzyk-Hordern B, Zioek M, Nawrocki J (2003) Catalytic ozonation and methods of enhancing molecular ozone reactions in water treatment. Appl Catal B46:639669 Kim IS, Park J, Kim K (2001a) Enhanced biodegradation of polycyclic aromatic hydrocarbons using nonionic
123
Rev Environ Sci Biotechnol (2006) 5:347374 surfactants in soil slurry. Appl Geochem 16:1419 1428 Kim J, Choi H (2002) Modeling in situ ozonation for the remediation of nonvolatile PAH-contaminated unsaturated soils. J Contam Hydrol 55:261285 Kim JH, Bae WK, Shim HJ, Shin HJ (2001b) PAH degradation characteristics under mixed conditions. Korean Groundwater and Soil Environment Society Meeting, Hanyang University, April 1314 Klausen J, Haderlein SB, Schwarzenbach RP (1997) Oxidation of substituted anilines by aqueous MnO2: effect of Co-solutes on initial and quasi-steady-state kinetics. Environ Sci Technol 31:26422649 Koran KM, Suidan MT, Khodadoust AP, Sorial GA, Brenner RC (2001) Effectiveness of an anaerobic granular activated carbon uidized-bed bioreactor to treat soil wash uids: a proposed strategy for remediating PCP/PAH contaminated oil. Water Res 35:23632370 Kulik N, Goi A, Trapido M, Tuhkanen T (2006) Degradation of polycyclic aromatic hydrocarbons by combined chemical pre-oxidation and bioremediation in creosote contaminated soil. J Environ Manag 78:382391 Kumada Y, Kisa T, Kuwano Y, Koshikawa H, Tashiro, Yasukagawa E, Shimizu Y (2005) Microbial community analysis of PAHs degradation in soil. Proc 5th KoreaJapan joint seminar on geo-environmental engineering, 4th July, Seoul National University, Seoul Kuwano Y, Shimizu Y (2006) Bioremediation of coal contaminated soil under sulfate-reducing condition. Environ Technol 27:95102 Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52:15391546 Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev54 (3):305315 Lee P, Ong S, Golchin J, Nelson GL (2001) Use of solvents to enhance PAH biodegradation of coal tar-contaminated soils. Water Res 16:39413949 Lee PH, Doick KJ, Semple KT (2003) The development of phenanthrene catabolism in soil amended with transformer oil. FEMS Microbiol Lett 228:217223 Lei L, Khodadoust AP, Suidan MT, Tabak HH (2005) Biodegradation of sediment-bound PAHs in eld contaminated Sediment. Water Res 39:349361 Liste H, Alexander M (2000) Plant-promoted pyrene degradation in soil. Chemosphere 40:710 Liste HH, Prutz I (2006) Plant performance, dioxygenaseexpressing rhizosphere bacteria, and biodegradation of weathered hydrocarbons in contaminated soil. Chemosphere 62:14111420 Luthy RG, Aiken GR, Brusseau ML, Cunningham SD, Gschwend PM, Pignatello JJ, Reinhard M, Traina SJ, Weber Jr W, Westall JC (1997) Sequestration of hydrophobic organic contaminants by geosorbents. Environ Sci Technol 31:33413347 Macleod CJA, Semple KT (2005) The inuence of single and multiple applications of pyrene on the evolution
371 of pyrene catabolism in soil. Environ Pollut 139:455460 Macleod CJA, Semple KT (2002) Evolution of pyrene catabolic ability in similar soils with different organic matter contents. Environ Pollut 119:357364 Maliszewska-Kordybach B, Smreczak B (2000) Ecotoxicological activity of soils polluted with polycyclic aromatic hydrocarbons (PAHs) effect on plants. Environ Technol 21:10991110 Mallakin A, Dixon DG, Greenberg BM (2000) Pathway of anthracene modication under simulated solar radiation. Chemosphere 40:14351441 Maruya KA Risebrough RW, Horne AJ (1996) Partitioning of polynuclear aromatic hydrocarbons between sediments from San Francisco Bay and their pore waters. Environ Sci Technol 30:29422947 Meckenstock RU, Annweiler E, Michaelis W, Richnow HH, Schink B (2000) Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:27432747 Meckenstock RU, Sanowski M, Griebler C (2004) Anaerobic degradation of polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol 49:2736 Moretto LM, Silvestri S, Ugo P, Zorzi G, Abbondanzi F, Baiocchi C, Iacondini B (2005) Polycyclic aromatic hydrocarbons degradation by composting in a soot-contaminated alkaline soil. J Hazard Mater 126:141148 Morimoto K, Tatsumi K (1997) Effect of humic substances on the enzymatic formation of OCDD from PCP. Chemosphere 34:12771283 Mulder H, Breure AM, Van Andel JG, Grotenhuis JTC, Rulkens WH (1998) Inuence of hydrodynamic conditions on naphthalene dissolution and subsequent biodegradation. Biotechnol Bioeng 57:145154 Namkoong W, Hwang E, Park J, Choi J (2002) Bioremediation of diesel-contaminated soil with composting. Environ Pollut 119:2331 Nedwell DB (1999) Effect of low temperature on microbial growth: lowered afnity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101111 hler M, Antranikian G (1999) Niehaus F, Bertoldo C, Ka Extremophiles as a source of novel enzymes for industrial application. Appl Microbiol Biotechnol 51:711729 Northcott GL, Jones KC (2001) Partitioning, extractability, and formation of non-extractable PAH residues in soil: compound differences in aging and sequestration. Environ Sci Technol 35:11031110 Ohkuma T, Kisa T, Kumada Y, Kuwano Y, Venkata Mohan S, Tanaka H, Shimizu Y (2006) Surfactant enhanced bioremediation of the soil contaminated by coal derived hydrocarbons Proc Geo-environmental Engineering 2006 (sixth JapaneseKoreanFrance joint seminar on geoenvironmental engineering), April 34, Kyoto University Oleszczuk P, Baran S (2003) Degradation of individual polycyclic aromatic hydrocarbons (PAHs) in soil polluted with aircraft fuel Polish. J Environ Stud 12:431437
123
372 OMahony MM, Dobson ADW, Barnes JD, Singleton I (2006) The use of ozone in the remediation of polycyclic aromatic hydrocarbon contaminated soil. Chemosphere 63:307314 Ortega-Calvo J, Saiz-Jimenez C (1998) Effect of humic fractions and clay on biodegradation of phenanthrene by a Pseudomonas uorescens strain isolated from soil. Appl Environ Microbiol 64:31233126 Ortega-Calvo JJ, Marchenko AI, Vorobyov AV, Borovick RV (2003) Chemotaxis in polycyclic aromatic hydrocarbon-degrading bacteria isolated from coal tar- and oil-polluted rhizospheres. FEMS Microbiol Ecol 44:373381 Pan B, Xing BS, Liu WX, Tao S, Lin XM, Zhang XM, Zhang YX, Xiao Y, Dai HC, Yuan HS (2006) Distribution of sorbed phenanthrene and pyrene in different humic fractions of soils and importance of humin. Environ Pollut 143:2433 Pandey GR, K Jain (2002) bacterial chemotaxis toward environmental pollutants: role in bioremediation. Appl Environ Microbiol 68:57895795 Parales RE, Harwood CS (2002) Bacterial chemotaxis to pollutants and plant-derived aromatic molecules. Curr Opin Microbiol 5:266273 Parales RE, Haddock JD (2004) Biocatalytic degradation of pollutants. Curr Opin Biotechnol 15:374379 Park JS, Wade TL, Sweet S (2001) Atmospheric distribution of polycyclic aromatic hydrocarbons and deposition to Galveston Bay, Texas, USA. Atmos Environ 35:32413249 Park JY, Cho HJ, Yang JW (2000) Effects of surfactant on electrokinetic remediation of soil contaminated by phenanthrene. Taejon/Chungnam-Kyushu, Serial 13, Fukuoka, Japan, pp 267268 Park KS, Sims RC, Dupont RR, Doucette WJ, Matthews JE (1990) Fate of PAH compounds in two soil types: inuence of volatilisation, abiotic loss and biological activity. Environ Toxicol Chem 9:187195 Parrish ZD, Banks MK, Schwab AP (2004) Effect of root death and decay on dissipation of PAHs in the rhizosphere of yellow sweet clover and Tall Fescue. J Environ Qual 34:207216 Parrish ZD, Banks MK, Schwab AP (2005) Assessment of contaminant lability during phytoremediation of polycyclic aromatic hydrocarbon impacted soil. Environ Pollut 137:187197 Phillips DA, Streit WR (1996) Legume signals to rhizobial symbionts: a new approach for dening rhizosphere colonization. In: Stacey G, Keen NT (eds) Plant microbe interactions. Chapman Hall, New York, pp 236271 Pignatello JJ, Xing B (1996) Mechanisms of slow sorption of organic chemicals to natural particles. Environ Sci Technol 30:111 Postma J, van Veen JA (1990) Habitable pore space and survival of Rhizobium leguminosarum biovar trifolii introduced into soil. Microb Ecol 19:149161 Reid BJ, Jones KC, Semple KT (2000) Bioavailability of persistent organic pollutants in soils and sediments perspective on mechanisms, consequences and assessment. Environ Pollut 108:103112
Rev Environ Sci Biotechnol (2006) 5:347374 Reid BJ, Fermor TR, Semple KT (2002) Feasibility of using mushroom compost for the bioremediation of PAH-contaminated soil. Environ Pollut 118:6573 Rentz JA, Alvarez PJJ, Schnoor JL (2005) Benzo[a]pyrene co-metabolism in the presence of plant root extracts and excudates: implications for phytoremediation. Environ Pollut 136:477484 Reilley MR, Muzzio FJ, Buettner HM, Reyes SC (1996) A simple correlation for predicting effective diffusivities in immobilized cell systems. Biotechnol Bioeng 49:223227 Rowland AP, Lindley DK, Hall MJ, Rossall MJ, Wilson DR, Benham DG, Harrison AF, Daniels RE (2000) Effects of beach sand properties, temperature and rainfall on the degradation rates of oil in buried oil/ beach sand mixtures. Environ Pollut 109:109118 Sabate J, Vinas M, Solanas AM (2006) Bioavailability assessment and environmental fate of polycyclic aromatic hydrocarbons in biostimulated creosote-contaminated soil. Chemosphere 63:16481659 Salanitro JP, Dorn PB, Huesemann MH, Moore KO, Rhodes IA, Jackson LM, Vipond TE, Western MM, Wisniewski HL (1997) Crude oil hydrocarbon bioremediation and soil ecotoxicity assessment. Environ Sci Technol 31:17691776 Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243248 Sartoros C, Yerushalmi L, Beron P, Guiott SR (2005) Effects of surfactant and temperature on biotransformation kinetics of anthracene and pyrene. Chemosphere 61:10421050 Sela R, Goldrat T, Avnimelech Y (1998) Determining optimal maturity of compost used for land application. Compost Sci Util 6:8388 Semple KT, Dew NM, Doick KJ, Rhodes AH (2006) Can microbial mineralization be used to estimate microbial availability of organic contaminants in soil? Environ Pollut 140:164172 Semple KT, Jones KC, Craven A (2005) Introductory remarks to the Special Issue. Environ Pollut 133:12 Semple KT, Doick KJ, Burauel P, Craven A, Harms H, Jones KC (2004) Dening bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ Sci Technol 38:228A231A Seung HW, Jeon CO, Park JM (2004a) Phenanthrene biodegradation in soil slurry systems: inuence of salicylate and Triton X-100. Korean J Chem Eng 21(2):412418 Seung HW, Lee MW, Park JM (2004b) Biodegradation of phenanthrene in soil-slurry systems with different mass transfer regimes and soil contents. J Biotechnol 110:235250 Shimp JF, Tracy JC, Davis LC, Lee E, Huang W, Erikson LE, Schnoor JL ( 1993) Benecial effects of plants in the remediation of soil and groundwater contaminated with organic materials. Crit Rev Environ Sci and Technol 23: 4177 Siciliano SD, Germida J J (1998) Mechanisms of phytoremediation: biochemical and ecological interactions between plants and bacteria. Environ Rev 6:6579
123
Rev Environ Sci Biotechnol (2006) 5:347374 Sijm D, Kraaij R, Belfroid A (2000) Bioavailability in soil or sediment: exposure of different organisms and approaches to study it. Environ Pollut 108:113119 Spain JC, Pritchard PH, Bourquin AW (1980) Effects of adaptation on biodegradation rates in sediment/water cores from estuarine and freshwater environments. Appl Environ Microbiol 40:726734 Spain JC, Van Veld PA (1983) Adaptation of natural microbial communities to degradation of xenobiotic compounds: effects of concentration, exposure time, inoculum and chemical structure. Appl Environ Microbiol 45:428435 Susarla S, Medina VF, McCutcheon SC (2002) Phytoremediation: an ecological solution to organic chemical contamination. Ecol Eng 18:647658 Suthersan SS (2002) Natural and enhanced remediation systems. CRC Press LLC Tang J, Carroquino MJ, Robertson BK, Alexander M (1998) Combined effect of sequestration and bioremediation in reducing the bioavailability of polycyclic aromatic hydrocarbons in soil. Environ Sci Technol 32:35863590 Tang Y, Qi JL, Krieger-Brockett B (2005) Evaluating factors that inuence microbial henanthrene biodegradation rates by regression with categorical variables. Chemosphere 59:729741 Taylor LT, Jones DM (2001) Bioremediation of coal tar PAH in soils using biodiesel. Chemosphere 44:1131 1136 Trindade PVO, Sobral LG, Rizzo ACL, Leite SGF, Soriano AU (2005) Bioremediation of a weathered and a recently oil-contaminated soils from Brazil: a comparison study. Chemosphere 58:515522 USEPA (1995) Cost and performance report: slurry phase bioremediation application at the Southeastern Wood Preserving Superfund Site Canton, Mississippi. Report contract Number: 68-W3-0001 USEPA (2003) Pilot scale demonstration of a slurry phase biological reactor for creosote contaminated soil application analysis report, EPA/540/A591/009, USEPA, Ohio Van Limbergen H, Top EM, Verstraete W (1998) Bioaugmentation in activated sludge: current features and future perspectives. Appl Microbiol Biotechnol 50:1623 Venkata Mohan S, Krishna Prasad K, Sarma PN (2004b) Oxidative enzyme catalyzed transformation of PAH in soil to enhance biodegradation. Proc international conference on soil and ground water contamination, risk assessment and remedial measures, NGRI, Hyderabad, December 811 Venkata Mohan S, Nancharaiah YV, Flankentof FC, Wattiau P, Wuertz S, Wilderer PA (2002) Monitoring the conjugal transfer of plasmid PWWO from Pseudomonas putida in sequencing batch biolm reactor. In: Proceedings of VAAM conference, Gottingen Venkata Mohan S, Shailaja S, Ramakrishna M, Reddy KB, Sarma PN (2006) Bioslurry phase degradation of DEP contaminated soil in periodic discontinuous mode operation: inuence of augmentation and substrate partition. Process Biochem 41:644652
373 Venkata Mohan S, Sirisha R, Sarma PN, Reddy SJ (2004a) Degradation of chlorpyrifos contaminated soil by bioslurry reactor operated in sequencing batch mode-bioprocess monitoring. J Hazard Mater 116:3948 Vervaeke P, Luyssaert S, Mertens J, Meers E, Tack FM, Lust N (2003), Phytoremediation prospects of willow stands on contaminated sediment: a eld trial. Environ Pollut 126:275282 Villemur R, Deziel E, Benachenhou A, Marcoux J, Gauthier E, Lepine F, Beaudet R, Comeau Y (2000) Two liquid phase slurry bioreactors to enhance the degradation of high molecular weight polycyclic aromatic hydrocarbons in soil. Biotechnol Prog 16:966972 Weber WJ, Huang W (1996) A distributed reactivity model for sorption by soils and sediments intraparticle heterogeneity and phase-distribution relationships under non-equilibrium conditions. Environ Sci Technol 30:881888 White JC, Kelsey JW, Hatzinger PB, Alexander M (1997) Factors affecting sequestration and bioavailability of phenenthrene in soils. Environ Toxicol Chem 16:20402045 White JC, Alexander M, Pignatello JJ (1999) Enhancing the bioavailability of compounds sequestered in soil and aquifer solids. Environ Toxicol Chem 182:182187 Whyte LG, Bourbonniere L, Bellerose C, Greer CW (1998) Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic Rhodococcus sp. Appl Environ Microbiol 64:25782584 Wilderer PA, Irvine RL, Goronszy MC (2001) Sequencing batch reactor technology. Scientic and Technical Report. IWA Publishing Willumsen PA, Karlson U (1997) Screening of bacteria, isolated from PAH contaminated soils, for production of biosurfactants and bioemulsiers. Biodegradation 7:415423 Woo SH, Park JM (1999) Evaluation of drum bioreactor performance used for decontamination of soil polluted with polycyclic aromatic hydrocarbons. J Chem Tech Biotechnol 74:937939 Woo SH, Park JM, Rittmann RE (2001) Evaluation of the interaction between biodegradation and sorption of phenanthrene in soil slurry systems. Biotechnol Bioeng 73:1124 Woo Y, Affourtit J, Daigle S (2004) A comparison of cDNA, oligonucleotide, and Affymetrix GeneChip gene expression microarray platforms. J Biomol Tech 15(4):276284 Wrenn BA Sarnecki KL, Kohar ES, Lee K, Venosa AD (2006) effects of nutrient source and supply on crude oil biodegradation in continuous-ow beach microcosms. J Environ Eng 132:7584 Xu R, Obbard JP (2003) Effect of nutrient amendments on indigenous hydrocarbon biodegradation in oil-contaminated beach sediments. J Environ Qual 32:1234 1243 Xu R, Lau NL, Lim YG, Obbard JP (2005a) Bioremediation of oil-contaminated sediments on an inter-tidal shoreline using a slow-release fertilizer and chitosan. Mar Pollut Bull 51:10621070
123
374 Xu R, Yong LC, Lim YG, Obbard JP (2005b) Use of slowrelease fertilizer and biopolymers for stimulating hydrocarbon biodegradation in oil-contaminated beach sediments. Mar Pollut Bull 51:11011110 Xu SY,Chen YX, Wu WX, Wang KX, Lin Q, Liang XQ (2006) Enhanced dissipation of phenanthrene and pyrene in spiked soils by combined plants cultivation. Sci Total Environ 363: 206215 Yuan SY, Wei SH, Chang BV (2000) Biodegradation of polycyclic aromatic hydrocarbons by a mixed culture. Chemosphere 41:14631468
Rev Environ Sci Biotechnol (2006) 5:347374 Zhao B, Zhu L, Li W, Chen B (2005)Solubilization and biodegradation of phenanthrene in mixed anionic nonionic surfactant solutions. Chemosphere 58:3340 Zheng Z, Obbard JP (2002) Polycyclic aromatic hydrocarbon removal from soil by surfactant solubilization and Phanerochaete chrysosporium oxidation. J Environ Qual 31:18421847 Zheng ZM, Obbard JP (2003) Oxidation of polycyclic aromatic hydrocarbons by fungal isolates from oil contaminated renery soil. Environ Sci Pollut Res 10:173176
123

Bioremediation Technologies

Enviado por

Dados do documento

Descrição original:

Direitos autorais

Formatos disponíveis

Compartilhar este documento

Compartilhar ou incorporar documento

Opções de compartilhamento

Você considera este documento útil?

Este conteúdo é inapropriado?

Direitos autorais:

Formatos disponíveis

Bioremediation Technologies

Enviado por

Direitos autorais:

Formatos disponíveis

Rev Environ Sci Biotechnol (2006) 5:347374 DOI 10.

Rev Environ Sci Biotechnol (2006) 5:347374

Chang et al. (2002)

Rev Environ Sci Biotechnol (2006) 5:347374

Oil eld-contaminated soil Diesel fuel-contaminated sediments

Gogoi et al. (2003) Boopathy (2003)

In situ Aerobic Aerobic Aerobic Aerobic Aerobic

Ex situ using land treatment units In situ

Ex situ, nutrients Aerobic Aerobic Aerobic Aerobic Aerobic Aerobic

Anaerobic, denitrifying conditions Aerobic

Coulon et al. (2005)

Table 1 continued Conditions Joner et al. (2001) Source of contaminant Reference

Mixed sward of clover and ryegrass

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

USEPA (2003) Seung et al. (2004a, b) Garon et al. (2004)

Aerobic Aerobic Aerobic

Fluorene-contaminated soil Phenanthrene- contaminated soil Diesel oil-contaminated soil

Garon et al. (2004) Woo et al. (2004) Biswas et al. (2005)

Ex situ, soil column bioreactor

Ex situ, soil column bioreactor Aerobic Aerobic Aerobic

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Microora Electron acceptor

Microbial metabolism rate

Microbial metabolism rate

Microbial metabolism rate

Soil properties Contaminant characteristics

Bioavailability Mass transfer Bioavailability Mass transfer Microbial metabolism rate

Rev Environ Sci Biotechnol (2006) 5:347374

Bioremediation system associated

Fig. 1 Factors associated with the bioremediation efciency of PAH-contaminated soil

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Other process integration with bioremediation

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Rev Environ Sci Biotechnol (2006) 5:347374

Você também pode gostar