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Biofouling: The Journal of Bioadhesion and Biofilm

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Role of hydrophobicity in bacterial adherence to

carbon nanostructures and biofilm formation
a b c a
Sonal Mazumder , Joseph O. Falkinham III , Andrea M. Dietrich & Ishwar K. Puri
a
Department of Engineering Science and Mechanics, Virginia Polytechnic Institute and State
University, Blacksburg, Virginia, 24061, USA
b
Department of Biological Sciences, Virginia Polytechnic Institute and State University,
Blacksburg, Virginia, 24061, USA
c
Department of Civil and Environmental Engineering, Virginia Polytechnic Institute and
State University, Blacksburg, Virginia, 24061, USA
Published online: 19 Jan 2010.

To cite this article: Sonal Mazumder , Joseph O. Falkinham III , Andrea M. Dietrich & Ishwar K. Puri (2010) Role of
hydrophobicity in bacterial adherence to carbon nanostructures and biofilm formation, Biofouling: The Journal of
Bioadhesion and Biofilm Research, 26:3, 333-339

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 Biofouling
Vol. 26, No. 3, April 2010, 333–339

Role of hydrophobicity in bacterial adherence to carbon nanostructures and biofilm formation

Sonal Mazumdera, Joseph O. Falkinham IIIb, Andrea M. Dietrichc and Ishwar K. Puria*
a
Department of Engineering Science and Mechanics, Virginia Polytechnic Institute and State University, Blacksburg, Virginia
24061, USA; bDepartment of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061,
USA; cDepartment of Civil and Environmental Engineering, Virginia Polytechnic Institute and State University, Blacksburg,
Virginia 24061, USA
(Received 11 August 2009; final version received 1 December 2009)
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The role of cell and surface hydrophobicity in the adherence of the waterborne bacterium Mycobacterium smegmatis
to nanostructures and biofilm formation was investigated. Carbon nanostructures (CNs) were synthesized using a
flame reactor and deposited on stainless steel grids and foils, and on silicon wafers that had different initial surface
hydrophobicities. Surface hydrophobicity was measured as the contact angle of water droplets. The surfaces were
incubated in suspensions of isogenic hydrophobic and hydrophilic strains of M. smegmatis and temporal
measurements of the numbers of adherent cells were made. The hydrophobic, rough mutant of M. smegmatis
adhered more readily and formed denser biofilms on all surfaces compared to its hydrophilic, smooth parent. Biofilm
formation led to alterations in the hydrophobicity of the substratum surfaces, demonstrating that bacterial cells
attached to CNs are capable of modifying the surface characteristics.
Keywords: bacterial adherence; Mycobacterium; hydrophobicity; carbon nanostructures; surface roughness; biofilm

Introduction mycobacteria including Mycobacterium smegmatis

Many nanotechnology applications require the assem-
bly of nanostructures along with biological entities,
such as cells, cellular substructures, and proteins and
enzymes, for example, for chemical synthesis or use as
biosensors. Nano- and microstructures can also occur
as artifacts of manufacturing processes on the abiotic
walls of catheters inserted into patients or in drinking
water distribution systems. In all of these cases, the
nanostructures can be colonized by bacteria, forming
biofilms that alter the performance characteristics
of these applications. In some anticipated applications
it would be desirable to enhance bacterial adherence
to nanostructures, eg when employing nanoscale
drug-, protein-, or chemical-delivery systems for
treating diseases and for detection of contaminants in
drinking water. Therefore it is important to identify the
factors that influence the adherence of bacteria to
nanostructures.
Bacteria are living colloidal particles that range
in size from about 0.2 mm to several micrometers in
length and about 1 mm in diameter. Bacterial cells
can possess relatively hydrophilic or hydrophobic
surfaces (Rosenberg 1984). Bacterial attachment to a
surface can occur through primary and reversible
adhesion, secondary and irreversible adhesion, and
biofilm formation (Dunne 2002). Nontuberculous
used for these experiments are normal inhabitants of
drinking water distribution systems and household
plumbing and high numbers are found attached to pipe
surfaces in biofilms (Falkinham et al. 2001; Torvinen
et al. 2004). The bacteria can be mobile or immobile on
the substratum during the adhesion process, which can
be either reversible or irreversible (Boks et al. 2009).
The initial reversible step involves weak forces, such
as van der Waals, electrostatic, and hydrophobic
interaction forces between the bacterial cell and
the substratum surface (Vanloosdrecht et al. 1987),
whereas a successive irreversible step occurs through
stronger covalent and hydrogen bonding forces, as well
as through cellular surface structures, such as flagella
and fimbraie (Goulter et al. 2009). Bacterial adhesion
to a surface can depend upon the presence of suitable
nutrients, surface charge and topology, and hydro-
phobicity (McLandsborough et al. 2006; Young 2006)
as has been shown for Mycobacterium avium (Carter
et al. 2003) and other mycobacteria (Williams et al.
2009) so that different substrata can produce dissimilar
biological responses (Dı́az et al. 2007; Morozan et al.
2007). However, there is considerable disagreement in
the literature over the past three decades regarding the
adhesion mechanics and the influence of various
factors on bacterial adhesion (Tang et al. 2009).

*Corresponding author. Email: ikpuri@vt.edu

ISSN 0892-7014 print/ISSN 1029-2454 online

Ó 2010 Taylor & Francis
DOI: 10.1080/08927010903531491
http://www.informaworld.com
 334 S. Mazumder et al.

While some studies point to the importance of the

substratum free surface energies in influencing bacter-
ial adhesion (Absolom et al. 1983), for example, by
increasing the surface roughness (Donlan 2002) and
hydrophobicity (Ludwicka et al. 1984; Paulsson et al.
1993; Brydon et al. 1996; Faille et al. 2002), others find
that although changing this energy by altering the
surface hydrophobicity influences the adhesion dy-
namics (Boks et al. 2009), there is no clear effect on
overall adhesion and biofilm formation (Vanpelt
et al. 1985; Bayoudh et al. 2006; Oliveira et al. 2006).
However, it is generally believed that microorganisms
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attach more rapidly to hydrophobic nonpolar surfaces

than to hydrophilic materials (Fletcher and Loeb 1979;
Pringle and Fletcher 1983; Bendinger et al. 1993;
Donlan 2002) above a threshold surface roughness
(Tang et al. 2009). Carbon nanostructures (CNs) can
be deposited on surfaces to make them super-hydro-
phobic (Lau et al. 2003; Journet et al. 2005; Lin et al.
2006; Naha et al. 2007), but the literature is sparse
on the response and adhesion of bacteria to them.
Depositing nanostructures on an initially smooth
surface creates microstructured unevenness that rough-
ens it by changing the surface topology. Increasing
roughness leads to increasing hydrophobicity due to
a Cassie effect when the surface tension of a water
droplet is supported by the rough bumps beneath it
(Naha et al. 2007). The objective in the present study
was to characterize the attachment of bacteria and the
consequent formation of a biofilm on nanostructured
surfaces of different hydrophobicity. CNs were depos-
ited on a variety of surfaces and the adherence and
biofilm formation of a representative waterborne
mycobacterium, M. smegmatis, measured.
Materials and methods
Synthesis and characterization of carbon nanostructures
The base substrata used in the experiment were
10 mm 6 10 mm square supports made from stainless
steel (SS) AISI 304 (Fe/Cr18/Ni 10) mesh from
0.25 mm diameter wires, SS AISI 302 (Fe/Cr18/Ni 8)
foils with a 0.1 mm thickness, and 4 mm 6 10 mm
silicon (Si) wafers (300 N/Ph (100) 1–10 O-cm 380 mm
SSP Prime). The CNs were deposited on these
substrata using a flame reactor, a schematic of which
is provided in Figure 1 (Sen and Puri 2004; Arana
et al. 2005; Naha et al. 2007). A co-annular axisym-
metric burner was used to generate a steady laminar
flame burning ethylene (99%) and laboratory air in a
4:1 ratio. The substrata were placed 10 mm above the
burner with an inner fuel flowrate of 0.269 l min71 and
an outer airflow of 31.7 l min71. The exposure time to
the flame in the reactor was 3 min for all samples.
Since the width of the substrata was much smaller than
Figure 1. Schematic of the flame reactor used for CN flame
synthesis.
that of the flame, only the inner flame core was
responsible for the nanostructure deposition. High
resolution Schottky field emission scanning electron
microscope (FESEM) images of the nanostructures
were obtained using a LEO (Zeiss) 1550 instrument at
a 5 kV accelerating voltage in the conventional high
vacuum mode.
Bacterial cells and growth, adherence and biofilm
measurements
M. smegmatis strain mc2155 and its spontaneous rough
mutant were used for the experiments. The rough
colony phenotype was stable upon long term cultiva-
tion and did not revert to the parent’s colony type. The
strains were grown to exponential phase in 1/10-
strength Brain Heart Infusion Broth (BHIB, Becton-
Dickenson, Sparks, MD) at 378C. BHIB was chosen
rather than a standard mycobacterial medium,
Middlebrook 7H9 containing oleic acid, because
of possible changes in the surface characteristics of
M. smegmatis due to oleic acid (Carter et al. 2003).
Following growth, cells were pelleted by centrifugation
(5000 6 g for 20 min), the supernatant medium
discarded, and cells suspended in the same volume of
sterile Blacksburg tap water. Cell number was mea-
sured as colony-forming units (CFU) on 1/10-strength
BHIB agar.
Multiple bare and CN-coated supports of all six
types were placed in a sterile plastic Petri dish
containing 20 ml of sterile Blacksburg tap water and
inoculated with *107 CFU of each bacterial suspen-
sion. The Petri dish was then gently agitated on a
 Biofouling 335

platform shaker at room temperature. After incuba-

tion for 1.5 h, the supports were transferred using
alcohol-flamed tweezers to another dish containing
20 ml of sterile Blacksburg tap water and washed
by gently swirling for 10 s. The washed support was
transferred into a tube containing 1 ml of sterile
Blacksburg tap water and vortexed at the highest
speed for 60 s. The recovery of cells was approximately
90% as judged by microscopic examination of
surfaces. The number of CFU in each suspension
was measured by spreading 0.1 ml in triplicate of each
suspension and a series of 10-fold dilutions. Following
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removal of supports for measurement of adherence,

the remaining supports with and without CNs were
incubated in the same cell suspension to permit biofilm
formation. After 13 days incubation at 308C, the
supports were gently washed and adherent cells
measured as described above. The results are reported
as mean CFU cm72 of surface (calculated on the
dimensions of the supports) of measurements from
three supports of the same type where the standard
errors were 510% of the values.

Measurement of bacterial cell and surface

hydrophobicity
Hydrophobicity of M. smegmatis cells was measured as
hexadecane adherence (Rosenberg 1984). Hexadecane
(0.1 ml) was added to 3 ml of cells suspended in sterile
Blacksburg tap water (*108 CFU ml71) and the
suspension vortexed at the highest speed for 60 s. The
aqueous and hexadecane layers separated after 60 min
and the absorbance of the aqueous layer was measured
at 540 nm. The percentage hexadecane adherence
was calculated as the difference in absorbance of the
untreated suspension minus the absorbance of the
hexadecane-treated suspension divided by the absor-
bance of the untreated suspension. The results reflect
the average (+standard deviation [SD]) of three
independent measurements. Surface hydrophobicity
was measured as the contact angles (both left and
right) of water droplets on bare and CN-coated
substrata, both before and after mycobacterial biofilm
formation, using a Kruss DSA 100 surface analyzer
(Kruss, USA). The results are reported as the mean +
the SD of the measured contact angles. This measure-
Figure 2. FESEM images of (a) a bare Si substratum
ment was performed three times (ie the number of
without mycobacteria, and substrata coated with CNs
samples n ¼ 3) without mycobacteria at (b) low and (c) high
magnifications after preparation.
Results and discussion
Substratum surface characterization
FESEM images of the different coated substrata CN-covered substratum surfaces. The nanostructured
revealed uniformly distributed CNs, as shown in coatings consisted of similarly agglomerated solid
Figure 2 that compares representative bare Si and particles or nanobeads. Their deposition occurred
 336 S. Mazumder et al.

during combustion through gas phase fuel pyrolysis in
the oxygen-deficient flame core. In this core, heavier
hydrocarbons were transported into the stagnation
layer adjacent to the relatively colder substratum
surface and condensed upon it to form the nanos-
tructures. The individual nanobeads ranged in size
from 24 to 51 nm (Naha et al. 2007).
In general, CN deposition increased the substratum
surface unevenness or roughness, thereby enhancing
the surface hydrophobicity by inducing a Cassie
equilibrium state. Water droplets in such a state sit
on the deposited nanostructured rough surfaces while
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and readily roll off the surface when disturbed (Naha
et al. 2007). The contact angle measurements that
characterize substratum surface hydrophobicity are
summarized in Table 1. For a water droplet placed on
an initially bare Si hydrophilic wafer, the contact
angle y  39.38. Once CNs were deposited on it, the
surface became hydrophobic due to the enhanced
surface roughness and y increased to *135.48. The
SS mesh was intrinsically hydrophobic and became
more so due to CN deposition with y increasing
from *102.2 to *138.48. This angle was roughly the
same for both a bare (y  77.18) and a CN-covered SS

air is entrapped in the voids in the underlying structure foil (y  79.28).

Table 1. Measurements of the contact angle y of water droplets with different substrata.

Sample y (8) Observation Characteristic Image

Bare Si wafer 39.3 + 0 Droplet smears surface Hydrophilic

CNs on Si wafer 135.4 + 0.3 Almost spherical droplet Highly hydrophobic

rolls off readily when
disturbed

Bare SS mesh 102.3 + 0.5 Droplet rolls off readily Hydrophobic

when disturbed

CNs on SS mesh 138.3 + 0.1 Almost spherical droplet Hydrophobicity increases

rolls off readily when
disturbed

Bare SS foil 77.1 + 1 Semicircular droplet Hydrophobic

CNs on SS foil 79.3 + 7 Semicircular droplet rolls Hydrophobicity increases

of readily when slightly
disturbed
 Biofouling 337

Table 2. Numbers of cells of M. smegmatis colony variants of wild type parent and rough mutant cells adhering to the substrata
after 1.5 h and in biofilms after 13 days incubation.

Wild type Rough

72
CFU cm CFU cm72
Surface y (8) 1.5 h 13 days 1.5 h 13 days
SS foil 77.1 Not detected 2.7 6 104 2.0 6 101 3.0 6 105
SS foil þ CNs 79.3 1.0 6 103 6.6 6 103 8.9 6 103 3.2 6 105
SS mesh 102.3 2.2 6 103 3.6 6 103 5.2 6 103 2.8 6 105
SS mesh þ CNs 138.3 3.8 6 103 2.0 6 103 5.4 6 103 3.2 6 105
Si 39.3 4.2 6 102 1.0 6 103 5.2 6 102 1.5 6 105
Si þ CNs 135.4 2.8 6 103 1.2 6 103 5.8 6 103 3.8 6 105
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Adherence of mycobacterial cells to nanostructures and
biofilm formation
Two colony wild type and rough cell variants of
M. smegmatis differed significantly in their cell surface
hydrophobicity as reflected by their adherence to
hexadecane in an aqueous medium, with wild type
adherence as 32 + 3% and rough adherence as
71 + 5%. The wild type parent was significantly
more hydrophilic towards water than the rough
mutant (Student’s t test, p 5 0.05). Both the wild
type and rough mutant cells adhered to the different
nanostructures upon short-term (1.5 h) exposure
to cells in suspension as shown through Table 2.
Starting with similar initial cell densities of 8.0 6 105
wild-type cells ml71 and 6.5 6 105 rough mutant
cells ml71 in suspension, a higher number of the
relatively hydrophobic rough cells adhered to the bare
and CN-coated substrata. (Only for the CN-coated
SS foil was the difference significant, p 5 0.05 by
Student’s t test, Table 2). However, far fewer bacteria
of either type adhered to bare Si and SS foil surfaces as
compared to the SS mesh and all three CN-coated
surfaces. Whereas, the bacterial adherence in the latter
cases was *103 CFU cm72, it was only *10–102 CFU
cm72 for the bare Si and SS foil surfaces. More cells of
either colony type adhered to the CN-coated surfaces
compared to the uncoated surfaces, but rough cell
attachment was typically higher than of the wild type
cells. As the total surface areas of the substrata were
likely different (eg foil vs grid), comparisons are
strongest between bare and CN-coated surfaces on
the same supports. Comparisons between attachment
of the colony variants to the different substratum
surfaces showed that when substantial bacterial
adherence (4103 CFU cm72) occurred, the proportion
of the more hydrophilic wild type parent cells that
adhered to the surfaces increased with surface hydro-
phobicity although the population of the more
hydrophobic rough cells was always higher.
The numbers of adherent cells were also measured
after 13 days incubation at 308C as is also shown in
Table 3. Contact angle measurements of water droplets on
CN-coated surfaces after biofilm formation by M. smegmatis
cells.
Contact angle, y (8)
After biofilm
Surface Bare surface formation
Silicon wafer 39.3 + 0.0 50 (wets surface)
Stainless steel mesh 102.3 + 0.5 77.1 + 0.5
Stainless steel foil 77.1 + 1.0 69.0 + 1.0
Table 2. The counts reflect the combined contributions
of adherence and growth of cells on the surfaces since
the CN-coated and uncoated surfaces were incubated
in the presence of cells in suspension. The data show
that substantial mycobacterial populations accumu-
lated on all the surfaces forming biofilms, but there
were significantly 10- to 100-fold higher numbers of
cells of the hydrophobic rough mutant (p 5 0.05,
Student’s t test). In most cases, while the number of
rough, hydrophobic mutant cells increased from *103
to *105 CFU cm72 over 1.5 h to 13 days, those of the
hydrophilic wild type parent cells remained somewhat
constant at *103 CFU cm72.
The hydrophobicity of the substratum surfaces was
again measured after these were covered with biofilms.
Mycobacterial biofilm formation due to M. smegmatis
cells substantially reduced the hydrophobicity of all
three CN-coated surfaces (Schaumann et al. 2007), as
shown in Table 3. Such a decrease in hydrophobicity
would be expected to change the binding character-
istics of CN-coated surfaces developed for various
applications.
Conclusions
The synthesis of hydrophobic CNs on different
substrata allowed measurements of the adherence
and biofilm formation by M. smegmatis cells. Surfaces
coated with CNs bound higher numbers of mycobac-
terial cells in the short term and formed denser biofilms
 338 S. Mazumder et al.
after incubation. The most striking result of the
measurements was that biofilm formation resulted in
substantial decreases in the hydrophobicity (character-
ized through the water-surface contact angle) of the
CN-coated surfaces.
Acknowledgments
Support from the Virginia Tech Institute of Critical
Technology and Applied Science to conduct this research,
and from Mr Steve McCartney of its Nanoscale Character-
ization and Fabrication Laboratory for help with SEM
images is gratefully acknowledged.
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