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Graduate School of Environmental Studies, Tohoku University, 6-6-06 Aza-Aoba, Aramaki, Aoba-ku, Sendai, Miyagi 980-8579, Japan
State Key Laboratory of Heavy Oil Processing, China University of Petroleum, PR China
c
College of Resources and Environment, Northwest A&F University, Yangling 712100, China
d
Department of Civil and Environmental Engineering, Graduate School of Engineering, Tohoku University, Japan
b
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
a r t i c l e
i n f o
Article history:
Received 9 April 2013
Received in revised form 14 November 2013
Accepted 26 November 2013
Available online 4 December 2013
Keywords:
Thermophilic methane fermentation
Methanogenesis
Wide range of ammonia
Microbial community
Chicken manure
a b s t r a c t
The thermophilic methane fermentation of chicken manure (CM) with a total solids (TS) of approximately
10% was investigated with regard to ammonia inhibition. A gradual increase in total ammonia nitrogen to
6000 mg/L was observed in the case of raw CM fermentation. A distinct rise in VFA accumulation combined with a low methane production of 0.29 L/gVS occurred at a TAN of 4000 5000 mg/L. Biogas production completely ceased when TAN reached 8000 mg/L after the addition of NH4HCO3. The high
sensitivity of methanogenesis to TAN and free ammonia (FA) was quantitatively conrmed. The IC50 of
TAN for methanogenesis, acidogenesis and hydrolysis was 5058, 5305 and 5707 mg/L at a pH value of
8.1 0.2. Similar results but with a lower IC50 were obtained for FA inhibition during fermentation.
The microbial community analysis revealed signicant differences in hydrogenotrophic methanogens
and aceticlastic methanogens before and after inhibition.
2014 Elsevier B.V. All rights reserved.
1. Introduction
Chicken manure (CM) is a typical agriculture waste with a high
fraction of biodegradable organic matter. In 2008, about 13 million
tons of CM was produced in Japan [1]. This huge amount of CM is
mainly treated by incineration and composting. However, due to
Corresponding author. Address: Graduate School of Engineering, Tohoku University, 6-6-06 Aza-Aoba, Aramaki, Aoba-ku, Sendai, Miyagi 980-8579, Japan. Tel.: +81
227957464; fax: +81 227957465.
E-mail address: yyli@epl1.civil.tohoku.ac.jp (Yu-You Li).
http://dx.doi.org/10.1016/j.cej.2013.11.074
1385-8947/ 2014 Elsevier B.V. All rights reserved.
588
more attention due to the high rate of biogas production, the short
hydraulic retention time (HRT) and improved pathogen destruction. Thermophilic fermentation has been applied to many cases,
such as sludge, municipal solid waste, cattle manure, poultry manure and corn grain ethanol industry waste treatment [46]. Compared with the mesophilic process, however, the thermophilic
process is more sensitive to changes in pH, VFA, ammonia and
toxic substrates. Nitrogen overloading has been shown to have a
signicant negative inuence on methanogenic activity, and can
render a reactor unstable. The TAN concentration of 3000
4000 mg/L is regarded to be at the edge of inhibition. Even at a
low TAN of 1700 mg/L, inhibition occurrence has been reported
[7]. Hashimoto reported that both thermophilic and mesophilic
processes are inhibited at a TAN of 2500 mg/L [8]. Thermophilic
fermentation has been reported to be unsuccessful for the relatively low nitrogen content in pig waste [9]. The fermentation of
swine manure as the sole substrate has been shown in earlier reports to be unsuccessful, mainly due to the high content of ammonia in the waste [8]. It has been shown that FA is a crucial fraction
of TAN for inhibition [10].
Individual volatile fatty acids (VFAs) can be used as process stability indicators in methane fermentation. Among them, butyrate
and isobutyrate acid have been shown to provide especially sensitive results [11]. Acetic and propionic acid were the most abundant
VFAs in manure digestion. VFA accumulated as Ammonia inhibition occurred, in effect indicating the extent of the inhibition.
It should be noted that CM is a high nitrogen content organic
waste with nitrogen levels much higher than those of cow manure,
food waste, pig manure and waste active sludge [12]. Hydrolysis in
thermophilic is faster than mesophilic which in itself makes CM
thermophilic fermentation a higher risk process [13]. More importantly, nitrogen inhibition is the result of chronic accumulation
during the operation of the reactor. The high concentration of
ammonium and volatile fatty acids (VFAs) tend to occur simultaneously, resulting in a stable pH. It was decided that the only
way to get convincing results on the chronic inhibition effect is
to operate the reactor in a long term.
Moreover, neither the whole performance nor the mechanism
of ammonium inhibition of thermophilic CM fermentation has
yet to be revealed in detail. Alternative methods of reducing the
nitrogen loading are by diluting CM to a low TS of 0.53% [14] or
mixing the CM with other livestock manure or sludge [15]. These
methods tend to increase the amount of nal discharged waste
water and result in a more complex process system. The effectiveness of high solid and sole CM fermentation needs further
investigation.
In the present research, a 240 days thermophilic fermentation
process using a continuous stirred tank reactor (CSTR) fed with
high solid CM was performed to investigate the followings: (1)
the methane yields from raw CM and ammonia stripping CM, (2)
the inhibition predisposing factor of high solid and high nitrogen
CM fermentation, (3) the effect of nitrogen inhibition on methanogenesis, acidogenesis and hydrolysis, (4) the microorganism community evolution before and after inhibition.
Table 1
Characteristics of raw CM and ammonia stripping CM.
Constituent
Unit
Average (n = 6)
SD ()
11.2
8.27
10.1
7.55
102,600
6450
3850
35.2
4.83
5.44
30.12
0.84
0.53
0.83
0.11
0.67
3200
810
200
0.45
0.05
0.24
0.18
0.10
Ammonia stripping CM
TS
(%)
VS
(%)
SS
(%)
VSS
(%)
T-COD
(mg/L)
TN
(mg/L)
TAN
(mg/L)
8.93
6.13
0.79
5.59
94400
3590
2500
0.144
0.197
0.049
0.046
8230
570
100
T-COD: total COD, TN: total nitrogen, TAN: total ammonia nitrogen, C:C element in
dry CM.
and ammonia stripping. The ammonia stripped CM, hereafter referred to as pretreated CM, and had a lower nitrogen substrate than
the Raw CM. Both the pretreated CM and raw CM were used in the
experiments respectively. The Total Solid (TS), Total Volatile Solid
(TVS), Total COD (TCOD), NH
4 N and Total Nitrogen (TN) were
analyzed to ascertain the stability of the substrate stability. The
characteristics of CM are given in Table 1.
2.2. CSTR operation procedure
A schematic diagram of the experimental device is provided in
Fig. 1. A lab-scale continuous stirred tank reactor (CSTR) with a
working volume of 12 L (total 15 L) was operated under thermophilic (55 1 C) conditions. The reactor was warmed by water circulation and agitated with a motor. A wet gas meter was used to
measure the daily biogas amount. The substrate tank was stirred
with 200300 RPM to keep the CM at a uniform semisolid state.
The TS content of the feedstock was adjusted to about 10% by adding tap water. The HRT was set at 30 days. The daily feedstock
amount was 0.4 L with OLR 0.21 kg/gd. The peristaltic inuent
pump with a timer was used to control the feeding at 12 times
per day to reduce feeding shock. Each feed was lower than 1% of
the reactor working volume. Seed sludge with TS of 3.1% was sampled from thermophilic anaerobic digestion of municipal sewage
treatment plant.
2.3. Analytical methods
The analyses of pH, alkalinity, COD, total ammonia nitrogen
(TAN), TS and TVS were performed according to Japan standard
methods [16]. The VFA concentration was determined by gas chromatography (Agilent-6890) equipped with a DB-WAXetr capillary
column (30 m 0.53 mm 1 lm) and an FID detector. The carrier gas
was Helium, with a pressure of 30.4 kPa, injected at a rate of
399 mL min1. The temperature of the injection port and detector
were 250 C and 250 C, respectively. The oven temperature was
set at 125180Cat a speed of 15 C min1.
Biogas was calibrated to that under standard conditions (0 C;
1.013 bar). The biogas composition was measured by a gas chromatograph (SHIMADZU GC-8A) equipped with a thermal
589
Hydrolysis %
Acidogensis %
Methanogenesis %
CODCH4
TCODin
TAN
10pH
4
!1
5
0:090182729:92
Tk
10
The effects of TAN and FA on hydrolysis, acidogenesis and methanogenesis were described and calculated using the extended
Boltzmann equation:
Y A2
A1 A2
1 expxx0
dx
ICi X0 dx LN
A1 A2
100 i A2 1
6
7
590
Fig. 2. The time course of biogas production, pH, VFA, and TAN content.
from 3689 mg/L to 70009000 mg/L. Consequently, readily consumable carbohydrate removal ratio dropped from 77% to 59%,
and the protein content dropped from 21% to 310%.
Throughout these three phases for 240 days, TAN continued to
accumulate, except during the rst stage when low nitrogen pretreated CM was used. After prolonged exposure to ammonia, the
TAN concentration reached 8000 mg/L resulting in a serious inhibition of the methane yield with a high VFA accumulation of
25000 mg/L. The total performance of CSTR is summarized in
Table 2.
Our results suggest that it is not possible to avoid inhibition
from ammonia in the thermophilic fermentation of raw CM with
high solid (about 10%) inuent. Long term operation was shown
to result in a high nal TAN concentration well in excess of the stable digestion limitation. Ammonium is a byproduct of the digestion
of organics and is produced together with biogas production. The
high biogas conversion and low TAN concentrations were in conict, and this was especially true in the case of high organic content
waste digestion. The reactor operation strategy was adjusted to accept low solid inuent rather than high solid.
3.2. The stoichiometry for methane fermentation of CM
The elemental composition of the raw CM was analyzed by dry
matter (see Table 1). The stoichiometric biochemical reaction
formula,
CnHaObNc + (n 0.25a 0.5b + 1.75c)
H2O ? (0.5n +
0.125a 0.25b 0.375c) CH4 + (0.5n 0.125a + 0.25b 0.625c)
CO2 + cNH4 + cHCO3 [23] was used to describe the element balance
and biogas conversion efciency. The stoichiometric formula was
identied as:
591
Unit
Phase 1
Phase 2a
Phase 2b
Phase 2c
Phase 3
(%)
(%)
(%)
(mg/L)
(L/g-VS)
(%)
(%)
3075 d
66.6
36.0
82.1
2830
0.32
61.75
37.6
75120 d
55.0
21.0
77.0
3700
0.28
51.01
47.1
120160 d
39.0
12.0
71.0
5170
0.18
39.27
56.8
160200 d
26.0
14.0
67.0
6000
0.13
40.59
57.9
200240 d
<19.0
3.010.0
59.0
70009000
0.05
34.17
63.8
CH4-COD/T-COD
VFA-COD/T-COD
S-COD/T-COD
P-COD/T-COD
(%)
(%)
(%)
(%)
66.5
4.5
6.1
23.0
55.1
4.7
6.2
33.8
38.6
10.3
15.1
36.1
26.2
30.3
5.5
37.8
13.5
29.6
3.2
53.7
4. Discussion
4.1. Effect of TAN on TCOD, protein and carbohydrate conversion
Since the carbohydrates, protein and lipids in organic waste are
known to have the largest contribution for methane fermentation,
it is important to reveal the extent to which they were degraded in
the fermentation process. Our focus was especially on protein and
carbohydrate degradation. The CM had a high protein content of
25% TS. In this study, protein, carbohydrate and TCOD removal
Fig. 3. Effect of TAN on the T-COD, protein and carbohydrate removal efciency.
592
to thousands depending on the substrate and the operation method. In this study, the signicantly inhibition concentration of FA
was about 1800 mg/L from the steady stage to the inhibited stage.
The methane fermentation of organic waste is a process involving three distinct stages; hydrolysis, acidogenesis, and methanogenesis. The methane fermentation process proceeds efciently
only when the degradation rates of all three stages are matched.
Different types of microorganisms characterize the three stages
and each presents a different sensitivity to ammonia inhibition.
The three stages of the biochemical reaction ratio are presented
in Fig. 5. A stable COD conversion during thermophilic digestion
was able to be maintained when TAN was below 4000 mg/L. The
COD, hydrolysis, acidogenesis and methanogenesis conversions
were 82%, 76%, 73% and 71%, respectively under stable conditions.
When the TAN concentration exceeded 4000 mg/L, methanogenesis conversion was the rst to drop. The half conversion ratio of
methanogenesis appeared at a TAN of 5058 mg/L. The acidogenesis
conversion began to decrease when the TAN concentration exceeded 5000 mg/L. The half conversion ratio of acidogenesis was
around 6000 mg/L. The hydrolysis ratio decreased from 76% at a
TAN of 5076 mg/L to 30% at a TAN of 6240 mg/L. When TAN
reached 6240 mg/L, the methanogenesis ratio decreased to 20%
while acidogenesis and hydrolysis ratio decreased to 25% and
32%. It could be concluded that methanogenesis was rstly and
readily inhibited, and that acidogenesis and hydrolysis conversion
declined in turn.
The three stage sequence of occurrences involved in inhibition
supported the principle of imbalance between the acetogenic and
methanogenic microorganisms, which differ signicantly in terms
of their physiology, nutritional needs, growth kinetics and sensitivity to environmental conditions. Hydrolysis and acidication could
run under a higher OLR and a low pH with a high biochemical reaction rate.
Fig. 4. Effects of TAN (a) and FA (b) on VFA and gas production.
593
Fig. 5. Simulation curve of TAN (a) and FA (b) effected on hydrolysis, acidogenesis and methanogenesis conversion ratio.
Table 3
Results of model fetting and calculation of IC10, IC50 and IC75 for Eq. (7).
Parameter
A1
TAN
Hydrolysis
Acidogenesis
Methanogenesis
A2
89.5 4.4
76.7 3.5
70.2 3.2
FA
Hydrolysis
Acidogenesis
Methanogenesis
89.5 7.5
80.7 3.7
70.2 6.1
x0
dX
IC10 (mg/L)
IC50 (mg/L)
IC75 (mg/L)
30 7.6
29 3.9
9.1 4.9
5494 202.6
5233 96.1
5277 112.2
311.7 1169.4
298.1 120.1
311.7 138.9
4817
4778
4244
5707
5305
5058
6292
5996
5603
20.2 17.9
16.0 6.7
4 9.6
2073 60.5
2101 28.4
2022 49.8
80.3 55.8
80.3 30.8
80.3 43.3
1944
1961
1839
2120
2115
2012
2291
2249
2083
The parameters and the calculated IC10, IC50 and IC75 are summarized in Table 3. The tting curves of hydrolysis, acidogenesis,
and methanogenesis are shown in Fig. 5a. Based on the simulation
results, the threshold of TAN on hydrolysis, acidogenesis, and
methanogenesis was over 8300 mg/L. With TAN inhibited methane
fermentation, hydrolysis was the most tolerant step while methanogenesis was the most sensitive and also the rst inhibited when
exposed to high nitrogen levels. The results also illustrate that following the increase of TAN, acidogenesis and hydrolysis were
inhibited in sequence and resulted in the failure of digestion. Those
results are consistent with the termination of gas production indicated in Fig. 4.
Fig. 5b illustrates the effect of FA inhibition on hydrolysis, acidogenesis, and methanogenesis. Obvious FA inhibition was noted
at levels of around 2000 mg/L among all three steps. The threshold
of FA on hydrolysis, acidogenesis, and methanogenesis were over
2500 mg/L. The IC10, IC50 and IC75 of FA for methanogenesis were
lower than those for both acidogensis and hydrolysis. In our study,
Table 4
Archaeal community in the thermophilic reactor of different stages.
Sampling stage (day)
No. of clones
No. of OTUs
Percentage (%)
Uitilization information
42
5
6
1
1
1
1
1
77.8
9.3
11.1
1.9
Total
54
100.0
19
1
1
1
95
5
Total
20
100.0
594
Table 5
Changes of bacterial community before and after inhibition.
Sampling stage (day)
Phylogenetic group
Firmicutes
Description
No. of OTUs
No. of clones
Percentage (%)
Natranaerobius thermophilus
Mahella australiensis
Peptoniphilus sp.
Alkaliphilus
Halothermothrix orenii
Ammonifex degensii
Moorella thermoacetica
Lactobacillus
Kurthia sp.
Tepidanaerobacter sp.
Thermoanaerobacter ethanolicus
Clostridium thermocellum
Dolosigranulum pigrum
Enterococcus
5
3
3
2
2
2
2
1
1
1
1
1
1
1
53
16
16
7
7
6
4
3
2
1
1
1
1
1
37.6
11.3
11.3
5.0
5.0
4.3
2.8
2.1
1.4
0.7
0.7
0.7
0.7
0.7
Citricoccus sp.
Corynebacterium
Propionibacterium
Streptomyces
2
2
2
1
3
3
3
1
2.1
2.1
2.1
0.7
Riemerella anatipestifer
Leadbetterella byssophila
Cytophaga hutchinsonii
1
1
1
3
2
1
2.1
1.4
0.7
Hylemonella gracilis
2.8
Actinobacteria
Bacteroidetes
Proteobacteria
Synergistetes
Anaerobaculum hydrogeniformans
1.4
39
141
100.0
Natranaerobius thermophilus
Clostridium thermocellum
Desulfotomaculum
Clostridium sporogenes
Halothermothrix orenii
Pelotomaculum thermopropionicum
Dethiobacter alkaliphilus
Turicibacter sanguinis
Ruminococcaceae bacterium
Syntrophothermus lipocalidus
Thermoanaerobacter
Enterococcus casseliavus
Eremococcus coleocola
Erysipelothrix rhusiopathiae
Moorella thermoacetica
Clostridium clariavum
Alkaliphilus metalliredigens
Pelotomaculum thermopropionicum
3
7
3
9
2
3
3
2
1
1
2
1
1
1
1
1
1
1
32
31
18
12
8
4
4
3
2
2
2
2
1
1
1
1
1
1
24.1
23.3
13.5
9.1
6.0
3.0
3.0
2.3
1.5
1.5
1.5
1.5
0.8
0.8
0.8
0.8
0.8
0.8
Pseudomonas stutzeri
Methylophaga sp.
1
1
1
2
0.8
1.5
Corynebacterium casei
2.3
Total
Firmicutes
After Inhibition (day 120)
Proteobacteria
Actinobacteria
Synergistetes
Anaerobaculum hydrogeniformans
Total
0.8
48
133
100.0
Under the stable fermentation condition, Methanoculleus marisnigri JR1 utilizing H2 + CO2, formate and dihydric alcohol was the
dominated methanogen. In the inhibited stage, Methanothermobacter thermautotrophicus str. increased to dominate methanogen
with 95% of archaea. Methanosarcina mazei Go1 was acetate acid
utilizing which occupied 11.1% of archaea in the steady stage but
it was not detected in the inhibited stage, proving that the VFA
accumulation involved is largely acetic acid accumulation as
showed in Fig. 4. The assumption that acetate utilizing
methanogens is the rate limiting step was consistent with the results in this study. The cloning sequencing results illustrated that
595
5. Conclusions
(1) A feasibility of CM fermentation was obtained feeding with
ammonia stripping CM and feeding with raw CM with TAN
below 4000 mg/L producing 0.74 m3/kg VSdegraded biogas
and 70.93 g/kg VSdegraded of ammonia nitrogen.
(2) The VFA accumulation was obviously at a TAN of 4000
5000 mg/L, and biogas was ceased at a TAN over 8000 mg/L.
(3) The IC10, IC50 and IC75 of TAN and FA on methanogenesis
were much lower than those for both acidogenesis and
hydrolysis.
(4) 16S r DNA cloning library resulted that aceticlastic M. mazei
Go1 occupied 11.1% of the methanogens in the steady stage
but not detected after inhibition, thus revealing serious VFA
accumulation.
Acknowledgements
The authors would like to acknowledge the technical cooperation in this investigation from Hitachi Engineering and Serves Co.
Ltd. The rst author was supported by China Scholarship Council
(CSC) for a scholarship.
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