annuk2010

c h a p t e r
39
Microbial biofilm-related polysaccharides
in biofouling and corrosion
Heidi Annuk and Anthony P. Moran
Summary Keywords: Biofilms; Capsular polysaccharides;

Exopolysaccharides; Slime; Extracellular polymeric
substances; Biofouling; Biocorrosion; Microbially
Understanding the mechanism of biofilm formation influenced corrosion
is the first step in determining its function and,
thereby, its impact and role in the environment. The
predominant components of biofilms are extracellular
polysaccharides, which account for approximately
90% of the enveloping matrix polymers that have
1. Introduction – biofilm
a significant impact on biofilm composition and systems
characteristics. The unwanted accumulation of biofilms
in the industrial setting is termed biofouling which
The biofilm mode of growth encompasses
includes biofilm formation in the domestic, industrial
surface-associated multispecies microbial com-
and health-related fields in various environments
such as cooling towers, water treatment systems, munities that are embedded in a matrix of extra-
paper mills and many surfaces within. In addition, cellular polymeric substances (EPS) (Donlan,
the metabolic activities of microbial cells on a metal 2002) and are associated with working materials,
surface can cause biocorrosion. Practically, every corrosion products, debris, soil, particles, etc.
industrial sector has accrued costs as a direct result In natural and man-made environments, bac-
of biofouling, such as decreased efficiency, increased teria predominantly live in biofilms on biotic
running costs, system damage or breakdown, and (e.g. tissue) or abiotic (e.g. plastic, metal, wood
deterioration in product quality. It is generally accepted or mineral) surfaces. The composition of EPS is
that greater knowledge of the structure and functions an important characteristic impacting on biofilm
of the extracellular polymeric substances, and their
strength, absorption capacity of biofilms for pol-
polysaccharide component in particular, would
lutants, microbial disinfectant resistance and
aid the development of methods to remove and/or
prevent biofilm formation. Thus, the present overview exo-enzyme degradation activity, which all affect
includes a general discussion of the contributions the behaviour of biofilms in technical systems
of polysaccharides in biofouling and, subsequently, (Moran and Ljungh, 2003). For example, the char-
examples of environmental and industrial problems acteristics of EPS are responsible for the erosion
caused by polysaccharides in biofilms are described. and sloughing from biofilms, frictional resistance
Microbial Glycobiology 781 © 2009

2010, Elsevier Inc.
782 39. Biofilm-related polysaccharides in biofouling
in pipes, adsorption of solids from bulk liquid which includes biofilm formation in domestic,
and clogging of filter membranes (Ceyhan and industrial and health-related fields in the var-
Ozdemir, 2008). In practice, biofilm formation ied environments of cooling water towers, heat
itself is not a problem, but the effects it can have exchangers, paper mills, food processing plants
on a process, e.g. decreased efficiency, increased and implanted medical devices (e.g. catheters,
running costs, system damage or breakdown, implants, prosthetics, etc.). In particular, the lat-
and deterioration in product quality, can have ter has been the subject of extensive reviews and
major implications (Patching and Fleming, 2003). intensive investigations (Habash and Reid, 1999;
A number of organisms, including bacteria, Donlan, 2001, 2002; Götz, 2002; Hall-Stoodley
protozoa, fungi, barnacles and other marine et al., 2004; Eiff et al., 2005; Tamilvanan et al.,
organisms, have been shown to form biofilms 2008), especially since this contamination can act
(Qian et al., 2007). Biofilms are innate to liquid– to spread opportunistic infections, e.g. device-
surface interfaces; all that is needed is a nutri- related infection with Staphylococcus epidermidis
tious environment for microorganisms to grow (Hall-Stoodley et al., 2004). Thus, biofilm for-
and produce biofilms. Single-species biofilms are mation not only on medical devices but also in
uncommon in the natural environment where mucosae should be considered as a virulence fac-
they are usually composed of a mixture of micro- tor (see review, Moran and Annuk, 2003). In addi-
bial species (Sutherland, 2001a). Furthermore, tion, the metabolic activities of microbial cells on
as biofilms occur in a large and varied number a metal surface can cause microbially influenced
of environments, the structural characteristics corrosion or so-called biocorrosion (Beech, 2003).
of any single biofilm formed, under a specific Practically, every industrial sector has
set of parameters, may be unique to that sin- accrued costs as a direct result of biofouling. It
gle environment and microflora (Sutherland, is generally accepted that a greater knowledge
2001b). Assuming this, within any biofilm, of the structure and functions of the EPS, and
there will almost certainly be wide varia- its PS component in particular, would aid the
tion in composition, including that of the EPS development of methods to remove and/or pre-
produced (Moran and Ljungh, 2003). As the prevent biofilm formation. Thus, excluding the role
dominant components of EPS are polysaccha- of biofilms in implanted medical device con-
rides (PSs), these will also vary in structure (see tamination (which as described above has been
Chapter 37). Their hydrophilic and polymeric reviewed extensively elsewhere), the present
structure provides a permeable matrix suitable chapter includes a general discussion of the con-
for cell growth in an aqueous environment, but tributions of PSs in biofouling and, subsequently,
also provides substantial mechanical properties examples of environmental and industrial prob-
(Moran and Ljungh, 2003). The function of EPS lems caused by biofilms are described and, in
and exopolysaccharides in biofilm formation has particular, the participation of PSs in these.
been reviewed in detail elsewhere (Sutherland,
2001a,b; Flemming and Wingender, 2001; Branda
et al., 2005). In general, PS chains have chemical 2. Biofilm-related PSs in
properties that make them polar and thus very
“sticky”, leading to surface adhesion and cell
biofouling and corrosion
cohesion (Sutherland, 2001a). Moreover, this is
one of the properties that makes biofilms diffi- Extracellular polymeric substances (mostly
cult to remove from surfaces. PSs) surrounding the cells of microorganisms
The unwanted accumulation of biofilms are a unique feature of biofilms. The PSs are
in an industrial setting is termed biofouling present as thin strands between the cells and the
IV. Biological relevance of microbial glycosylated components

2. Biofilm-related PSs in biofouling and corrosion 783
surface, or as sheets of amorphous material on a 2001), however, the nature of these is differ-
surface, entrapping minerals or host-produced ent (Sutherland, 2001a). It is common for a
serum components (Donlan, 2001). given bacterial species to produce one or two
Extracellular PSs can be divided into capsu- different PSs, but rarely both at the same time
lar and exopolysaccharides according to separa- (Sutherland, 2001b). Concerning adhesion, vari-
tion by centrifugation of shaken liquid cultures. ous microbial EPS-containing PSs, proteins and
Capsular polysaccharides (CPSs) remain lipids have affinity for hydrophobic (low sur-
cell-associated, whereas cell-free supernatant face energy) substrates, whereas acidic and neu-
contains exopolysaccharides. However, with tral PSs prefer attachment to hydrophilic (high
biofilms this delineation is not so easy as many surface energy) materials (Beech et al., 2005).
of the extracellular PSs produced in biofilms are Bacteria in biofilms produce exopolysac-
insoluble, complicating the precise determina- charides that influence the corrosion behaviour
tion of their chemical structures (Branda et al., of metals by providing a matrix with sites for
2005). Nevertheless, PSs generally are a main aeration, ion-concentration and metal-binding
proportion of the dry matter of biofilms and (Majumdar et al., 1999) and affect their capac-
play major roles in determining the physical ity to concentrate metal ions from surfaces and
properties and structures of microbial biofilms bulk media. Binding of metals has importance
(Flemming and Wingender, 2001). Sutherland in both passivation and activation reactions; a
(2001b) speculated that the PS components of good example is biofilm production by the PS-
biofilms of microbial origin differ from those producer Delya marina which has been shown
produced by planktonic bacteria due to minor to induce almost complete passivation of mild
structural differences, e.g. the degree of acetyla- steel by 95% reduction of the corrosion rate
tion or their molecular mass, leading to their (Ford et al., 1988).
altered physical properties which can cause a The capacity of EPS to bind metal ions is
change in viscosity or gel-forming capacity. In important in the development of corrosion
addition, considering the environmental differ- (Kinzler et al., 2003). These mechanisms are
ences between the niches which bacteria inhabit reviewed in detail in Beech and Sunner (2004).
and the heterogeneous PSs produced, there can In summary, exopolysaccharide-associated func
be a wide disparity in biofilm structure, hence tional groups (e.g. carboxyl, phosphate, sulfate,
all analysed samples have extensive variations glycerate, pyruvate and succinate groups) have
in composition. a high affinity towards certain metal ions (e.g.
Biofilm chemical composition and exopoly- Ca2, Cu2, Mg2and Fe3) in different oxida-
saccharide production of surface-associated bac- tion states, which can cause shifts in standard
teria is dependent on their growth phase and reduction potentials. Such EPS-bound metal
nutrient status of the environment (Majumdar ions can open up new redox reaction pathways,
et al., 1999). Furthermore, all bacterial species like direct electron transfer from the metal
may excrete chemically and structurally different (e.g. iron) or a biomineral (e.g. FeS) which,
exopolysaccharides. For example, extracellular with a suitable electron acceptor (e.g. oxy-
PSs have been shown to be distinct to a particu- gen or nitrate in aerobic or anaerobic systems,
lar genus (e.g. pseudomonads), or can be even spe- respectively), can cause cathodic depolariza-
cies-specific (e.g. Escherichia coli) (Lindberg et al., tion and, consequently, increased corrosion. A
2001). Also, production of analogous extracellu- good example of the process is a study of iron
lar PSs by different microorganisms have been hydroxide-encrusted biofilms by Chan et al.
observed, e.g. alginate by Pseudomonas aerugi- (2004), which showed that bacterial exopoly-
nosa and by Azotobacter vinelandii (Nivens et al., mers could act as a base for the accumulation

of akaganeite (-FeOOH) pseudo-single crys- aureus and S. epidermidis, respectively (Danese

tals through ferric iron-binding with carboxylic et al., 2000; Kaplan et al., 2004; Chang et al.,
groups on the polymer. These authors proposed 2007). These linkages between the subunits of
that the production of the exopolymer was the polymers provide a functional specificity to
for precipitating iron oxyhydroxide mineral biofilm EPS and investigation of these particular
outside the microbial cell in a process required structures would aid development of techniques
for metabolic energy generation. In conclu- to control biofouling in the marine environment.
sion, these processes would assist the cathodic Furthermore, Jain and Bhosle (2008) studied
reaction with biominerals, thereby acting as cell attachment and formation of biofilms by a
electron-conducting fibres within the biofilm marine Pseudomonas sp. strain and showed the
(Beech et al., 2005). presence of calcofluor-binding and cellulase
Exopolysaccharides have been shown to con- sensitive -(1→4)-linked polymers, as well as
tain uronic acid which endows the molecules -d-glucose (Glc) and -d-mannose (Man) in
with acidic properties and an overall nega- the biofilm matrix. A role for these polymers in
tive surface charge; the latter is important in the formation and maintenance of biofilms of
PS metal-complexing capacity. For example, Pseudomonas fluorescens, E. coli, Salmonella enter-
alginates that are negatively charged and rich ica sv. Enteritidis, S. enterica sv. Typhimurium
in uronic acids have a high metal-complexing and Yersinia pestis also has been reported (Zogaj
capacity (Majumdar et al., 1999). In addition, et al., 2001; Darby et al., 2002; Spiers et al., 2002;
uronic acid has been shown to be the main com- Solano et al., 2002).
ponent of Klebsiella pneumoniae CPS (Balestrino Hexoses and pentoses are the main build-
et al., 2008). Moreover, a deficiency in uronic ing blocks of the biofilm PSs, but the exact
acid production by capsular mutants has been monosaccharide content is dependent on envi-
shown to influence K. pneumoniae initial adhe- ronmental conditions (e.g. nutrients) and this
sion to medical devices (Balestrino et al., 2008). variable monosaccharide composition influ-
Additionally, exopolysaccharides with a signifi- ences also physicochemical properties of the PS
cant amount of uronic acid show a high copper- (Bhaskar and Bhosle, 2005), e.g. arabinose (Ara)
binding capacity, which would be important to is important for cell aggregation (Bahat-Samet
microorganisms for growing on surfaces coated et al., 2004) and deoxy sugars like fucose (Fuc)
with toxic and anti-fouling compounds, e.g. and rhamnose (Rha) from diatom EPS contrib-
cuprous oxide (Majumdar et al., 1999). In addi- ute to foaming and flocculation (Zhou et al.,
tion, in marine environments where biocorrosion 1998). Furthermore, EPS produced by micro-
occurs, bacterial and microalgal EPS may contain organisms on submerged surfaces in aquatic
up to 20–25% uronic acids (Nichols and Nichols, environments are generally rich in monosac-
2008). Furthermore, the acidic PSs in the biofilms charides, like Glc and Man, which may serve
tend to ionize metals, thereby causing thinning as cues for the settlement and colonization of
of metal structures (Bhaskar and Bhosle, 2005). surfaces by macrofoulers such as barnacles,
The EPS in biofilms has several different func- oysters, mussels etc. (Bhaskar and Bhosle, 2005).
tions, but protection and maintenance of matrix These problems of biofouling are most common
structure appears to be the most important on ship hulls, navigational buoys, underwater
(Moran and Annuk, 2003; Jain and Bhosle, 2008). equipment, seawater piping systems, beach well
Examples are colanic acid with -(1→3)-, algi- structures, industrial intakes, ocean thermal
nate with -(1→4)- and PS intercellular adhesin energy conversion plants, offshore platforms,
(PIA) with -(1→6)-linkages which are pro- moored oceanographic instruments and sub-
duced by E. coli, P. aeruginosa and Staphylococcus marines (Azis et al., 2003). Importantly, biofilm

3. Biofouling causing environmental and industrial problems 785
layers on a ship’s hull can increase mass and forming metal ion bridges and hydrogen bonds
hydrodynamic drag, increasing fuel costs by up (Mopper et al., 1991). Consequently, TEPs tend to
to 15% (Molino and Wetherbee, 2008). Moreover, be very sticky, producing attachment upon colli-
acetylated sugar moieties have been found of sion, thus assisting biofilm development on the
importance in biofilm initiation and cell adhe- surfaces of filtration membranes used in water
sion (Tsang et al., 2006). For example, poly-- treatment plants. Additionally, TEPs may be
(1→6)-N-acetyl-d-glucosamine (GlcNAc) from the cause of biofouling of various infrastructure
staphylococci, a PS related to slime and bio- installations such as water delivery pipes, cool-
film production, mediates cell adherence to ing towers, etc.
biomaterials (Sadovskaya et al., 2005). As well,
polymer-containing GlcNAc plays a criti-
cal role in the adhesive force of the holdfast of
Caulobacter crescentus, the common stalked bac- 3. Biofouling causing
terium, which is among the first to colonize environmental and
submerged surfaces in aquatic environments. industrial problems
The attachment between the PS component at
the base of the stalk and a glass surface is one of
the strongest biological adhesions measured to 3.1. Contamination of cooling tower
date (Tsang et al., 2006). Moreover, Verhoef et al. systems
(2005) showed the presence of O-acetyl groups
Cooling towers are important for various
in 50% of all EPSs in a large variety of paper
industrial plants, such as petrochemical and
mill slimes in addition to the 63% presence of
wastewater treatment facilities (Bott, 1998).
uronic acid and pyruvate. The authors sug-
Biofouling of these systems causes severe eco-
gested that collectively these are responsible for
nomical loss by influencing the efficiency of
the hydrophobic and strong polyanionic nature
the respective process in the following ways
of particular EPSs, and are important factors for
(Patching and Fleming, 2003):
facilitating the involvement of EPSs in surface
attachment and playing a central role for the (i) hindrance of water flow by the biofilm
structural unity of a biofilm. because of occlusion of pipes and channels
Another PS complex, termed transparent and high frictional resistance with a
exopolymer particles (TEPs), plays a role in bio- requirement for additional pumping and
film formation and biofouling in the aqueous replacement costs (Michael, 2003).
environment and is ubiquitous in large quantities (ii) loss of heat transfer because of the
in both marine and freshwaters (Passow, 2002). biofilm having a low thermal conductivity
The TEPs, composed of acidic PSs, are one type of (Flemming, 2002; Tanji et al., 2007).
EPS produced by both diatoms and bacteria dur- (iii) biocorrosion caused by sulfate-reducing
ing their growth (Bhaskar and Boshle, 2005). The bacteria in an anaerobic biofilm layer and
properties of these small (2–200 m), negatively microbial biodeterioration of concrete and
charged, mostly PS particles implies their poten- wood in cooling towers (Prince et al.,
tial to play a role in the initiation and growth 2002).
of biofilms. By definition, TEPs are deformable, (iv) finally, biofilms can act as reservoirs
gel-like particles suspended in the water body for pathogens including Legionella spp.
and may be considered a “planktonic” sub- (Dondero et al., 1980; Garcia-Fulgueiras
group of EPS (Wotton, 2004). Highly surface- et al., 2003; Türetgen and Cotuk, 2007;
active PSs are responsible for these particles Nygård et al., 2008).

Because of the warm temperatures and con- (Türetgen and Cotuk, 2007). Previous stud-
tinual flow of nutrients, cooling towers are a ies have shown that Legionnaires’ disease
prime environment for the build-up of micro- outbreaks originate from cooling tower and
organisms. Ceyhan and Ozdemir (2008) stud- air-conditioning contamination by Legionella
ied biofilm samples from stainless steel cooling pneumophila (Dondero et al., 1980; Garcia-
water towers for chemo-organotrophic bac- Fulgueiras et al., 2003; Türetgen and Cotuk, 2007;
teria and found that species isolated from Nygård et al., 2008). Bacterial biofilm devel-
cooling water towers were Gram-negative non- opment is common on heat-transfer surfaces
spore forming and catalase-positive bacteria of cooling towers because of the higher tem-
(Table 39.1). They showed that all the isolated peratures present, which also favours the rapid
Pasteurella spp. had the highest production of growth of L. pneumophila (Harris, 2000). Rogers
PSs, with similar monosaccharide compositions et al. (1994) studied the influence of the plumb-
of Glc, d-galactose (Gal), Man, Rha and ribose ing materials on biofilm formation and growth of
(Rib). Of note, four pseudomonads produced L. pneumophila and found the lowest total
PSs with similar monosaccharide compositions flora on stainless steel. In contrast, a study by
and most extracellular PSs were enriched in Türetgen and Cotuk (2007) reported that poly-
Gal and Glc, but with lesser amounts of Man, ethylene and polyvinyl chloride supported sig-
Rha, fructose (Fru) and Ara; the EPS formed by nificantly low heterotrophic bacterial numbers,
Burkholderia spp. consisted mainly of Gal, Glc, whereas heterotrophic bacterial counts and
Man, Ara, Rha and Rib (Ceyhan and Ozdemir, those of L. pneumophila on galvanized steel were
2008). Consequently, as has been discussed, bio- significantly higher than those on other materi-
film formation occurs in a nutrient-rich environ- als. Nevertheless, Rogers et al. (1994) showed
ment, especially production of EPSs with a high that L. pneumophila accounted for a low propor-
PS content and, accordingly, Zhang and Bishop tion of biofilm flora on polybutylene and chlo-
(2003) have postulated the hypothesis that EPS is rinated polyvinyl chloride, but no growth was
biodegradable and that mixed microbial cultures observed on copper surfaces; hence, it was con-
will degrade their own EPS material when they cluded that the copper material in water systems
are in a starved state. This hypothesis has been could limit the colonization of L. pneumophila. In
supported by investigations (Ruijssenaars et al., addition, Assanta et al. (1998) showed a similar
1999; Rättö et al., 2001). In addition, Ceyhan and tendency of Aeromonas hydrophilia which pref-
Ozdemir (2008) observed that some bacterial erentially colonized polybutylene, a hydropho-
species were able to utilize EPS from Burkholderia bic surface, followed by stainless steel, but with
cepacia, Pseudomonas spp. and Sphingomonas pau- only a few cells attached to copper surfaces.
cimobilis, with the greatest viscosity reduction of Furthermore, Türetgen and Cotuk (2007) also
B. cepacia induced by a Pseudomonas spp., thus evaluated the quantity of EPS in biofilms by
showing that the bacteria in this particular sys- measuring carbohydrate content and showed
tem were able to degrade EPS from biofilms in that it was higher on galvanized steel and low-
cooling towers. Hence, some microorganisms est on polyvinyl chloride surfaces. In summary,
could be potential agents for the biodegradation the corrosivity of galvanized steel in the aque-
and bioconversion of wastes from agricultural, ous environment results in more extensive cor-
agro-industrial and food processing industries rosion products or surface area available for
(Kumar and Takagi, 1999). colonization. Thus, due to the rough corroded
A range of materials can be used for layer, galvanized steel may provide a suitable
tower manufacturing, but mainly galvanized niche for microorganisms for rapid biofouling
steel, stainless steel and concrete are applied (Pasmore et al., 2002).

Table 39.1 Genera of microorganisms found in different industrial environments
Environment Genera of microorganisms Reference
Cooling tower Burkholderia, Pseudomonas, Pasteurella, Alkaligenes, Aeromonas, Ceyhan and Ozdemir, 2008
Pantoea, Sphingomonas
Reverse osmosis Acinetobacter, Bacillus/Lactobacillus, Pseudomonas/Alcaligenes, Ridgway et al., 1983
membrane Flavobacterium/Moraxella, Micrococcus, Serratia
Reverse osmosis Bradyrhizobium, Rhodopseudomonas, Sphingomonas, Bacillus/ Chen et al., 2004
membrane Clostridium
Reverse osmosis Corynebacterium, Pseudomonas, Bacillus, Artrobacter, Baker and Dudley, 1998
membrane Flavobacterium, Penicillium, Trichoderma, Mucor, Fusarium,
Aspergillus; yeasts – occasionally
Nanofiltration membrane Pseudomonas/Burkholderia, Ralstonia, Bacteroides, Sphingomonas Ivnitsky et al., 2007
Microfiltration membrane Rhizobium, Agrobacterium, Zoogloea, Mesorhizobium, Caulobacter, Chen et al., 2004
Bradyrhizobium, Bosea, Aureobacterium, Brevibacterium,
Gordonia, Bacillus, Staphylococcus, Bordetella, Stenotrophomonas,
Flavobacterium
MBR HDO-MBR: Pandoraea, Bacillus, Sphingomonas, Citrobacter, Kim et al., 2006
Kluyvera
LDO-MBR: Azospirillum, Flavobacterium, Acinetobacter,
Rhizobium, Stenotrophomonas, Haliscomenobacter
Concrete Cyanobacteria – Phormidium, Leptolyngbya, Calothrix Barberousse et al., 2006c
Algae – Klebsormidium, Stichococcus, Chlorella, Bracteacoccus,
Geminella
Concrete Pseudomonas, Bacillus, Micrococcus, Moraxella, Anthrobacter, Maruthamuthu et al., 2008
Streptococcus, Staphylococcus, Acinetobacter
MBR, membrane bioreactor; HDO, high dissolved oxygen; LDO, low dissolved oxygen.
3.2. Biofouling in membrane-related molecules and can be applied for pretreatment

of water for NF or reverse osmosis (Rosberg,
processes
1997). Nanofiltration is a process selected when
Reverse osmosis, ultrafiltration, nanofiltra- reverse osmosis and ultrafiltration are not the
tion (NF) and microfiltration are widely used to ideal choice for separation and is used for dem-
separate suspended or colloidal and dissolved ineralization, desalination and also in drinking
(i.e. all other) materials from water solutions water purification process steps, such as water
in numerous industrial, medical and drinking softening, decolouring and micropollutant
water supply applications. Reverse osmosis is removal (Schaefer et al., 2004). Microfiltration
a high-pressure, energy-efficient technique for is a low-pressure cross-flow membrane proc-
dewatering process streams, concentrating low- ess for separating colloidal and suspended
molecular-mass substances in solution or puri- particles and is used for fermentation broth clar-
fying wastewater. Ultrafiltration is a pressurized ification and biomass clarification and recovery
membrane separation process used for remov- (Cheryan, 1998). Another system used for water
ing high-molecular-mass substances, colloidal purification is the membrane bioreactor (MBR).
materials, and organic and inorganic polymeric This system uses a combination of a membrane

process like microfiltration or ultrafiltration periods of shutdown or storage, primarily

with a suspended growth bioreactor, and is now caused by fungal species (Murphy et al.,
widely used for municipal and industrial waste- 2001). Such contamination of the pure water
water treatment (Judd, 2006). on the permeate side will occur during no-
In membrane systems, biofouling represents or low-flow periods because of the growth
a major problem as organic and inorganic dis- of bacteria through the membrane.
solved substances and particles can be removed
by pretreatment, but various microorganisms Flux decline caused by the activity of micro-
present on the surface of the membrane (see organisms on membrane surfaces is one of
Table 39.1) can multiply at the expense of bio- the major problems in membrane facilities
degradable substances in the water (Flemming (Ridgway and Flemming, 1996; Vrouwenvelder
et al., 1997). Once microorganisms attach to a et al., 1998; Al-Ahmad et al., 2000). Fonseca et al.
membrane, formation of a biofilm starts within (2007) studied EPS influence on the flux decline
hours. The type and growth rate of bacteria of model nanofiltration membrane systems. The
forming the biofilm is dependent on feed-water authors showed that membrane flux decline
composition, available food source and the was associated with an increase in surface extra-
presence or absence of a biocide. In addition, cellular PS mass since 30–80% of normalized
the extent of biofilm formation depends on the flux decline was observed when membrane-
surface material, smoothness, nutrients, water associated extracellular PS content increased
properties (e.g. temperature and pH) and sys- from 5 to 50 g/cm2. Above this PS level, higher
tem design characteristics (e.g. flow and pres- surface-associated PSs did not result in a signifi-
sure) (Mulder, 1996; Chang et al., 2002). cant increase in flux decline, thus indicating a
The problems caused by biofilm formation in surface saturation effect concerning the hydro-
membrane-related processes have been summa- dynamics through the mature biofilm.
rized by Patching and Fleming (2003): Furthermore, Herzberg and Elimelech (2007)
studied the biofouling mechanisms of reverse
(i) an increased hydraulic resistance can osmosis membranes and the impact of biofoul-
cause elevated pumping costs, lower ing on membrane performance with a model
permeate productivity, increase cleaning bacterial strain, P. aeruginosa PA01 under accel-
intervals and induce potential membrane erated biofouling conditions. They showed that
damage (Chang et al., 2002; Herzberg and the drastic flux decline caused by the deposited
Elimelech, 2007). bacterial cells on the membrane was lower than
(ii) biofouling of the feed channel spacers in that caused by biofilm growth, despite the very
desalination plants results in a pressure high cell concentration added to the unit. It was
drop between the feed and brine lines shown that the additional decrease in permeate
(differential pressure, P) leading to flux in the presence of the biofilm was caused by
increased salt passage and, consequently, the hydraulic resistance produced by EPS. The
an impure product. The biofilm layer authors suggested that the EPS matrix between
entraps salts and prevents the turbulent the cells can give hydraulic resistance to perme-
flow from thoroughly mixing the solutes ate flow, comparable to fouling of reverse osmo-
in the feed stream, thus causing a sis membranes by PSs, such as alginate (Ang
“concentration polarization” effect (Paul et al., 2006). With membrane biofilms, increased
and Abanmy, 1990). hydraulic resistance (P) has often been attrib-
(iii) cellulose acetate membranes are disposed uted to the viscoelastic properties of biofilms
to biofilm-related degradation during (Baker and Dudley, 1998). The physical structure

of biofilms found in membrane systems can be anoxic biofilm. similar tendencies were observed
compact and “gel-like” or “slimy and adhesive” by Kim et al. (2006) who showed that the rate
(Ye et al., 2005), with some consisting of a high of membrane fouling for a low dissolved oxy-
ratio of PS slime to viable microorganisms, i.e. gen (LDO-) MBR was faster than that for a high
106–108 colony forming units of bacteria per cm2 dissolved oxygen (HDO-) MBR, although the
of membrane (Baker and Dudley, 1998). thickness of the fouling layer was greater in the
In addition, Haberkamp et al. (2008) investi- latter. In addition, the biofilm in the LDO-MBR
gated the impact of EPS on ultrafiltration mem- contained a larger amount of EPS than that in
brane fouling in tertiary sewage treatment by the HDO-MBR, with the latter having a higher
addition of an EPS mixture to different test solu- protein to PS ratio in the biofilm. The microbial
tions. The flux decline induced by bacterial EPS communities have been shown to differ between
was influenced by the formation of a rather loose- the HDO- and LDO-MBRs, which likely explains
bound, polarized concentration layer of large the different structures and permeabilities of the
PSs, whereas the secondary effluent fouling layer respective biofilms.
consisted of the tighter adhesion of macromol
ecular substances with a variety of biopolymers
present. However, ultrafiltration of the second-
3.3. Biofouling of concrete
ary effluent resulted in a higher flux decline than
ultrafiltration of the EPS model solutions. Various microorganisms such as bacteria, fungi,
The influence of EPS on membrane fouling algae and lichens are found to be important in con-
in the MBR system was studied by Rosenberger crete biodeterioration (see Table 39.1) (Gaylarde
et al. (2006) who compared differences in mem- et al., 2003). Green microalgae and cyanobacte-
brane performance between two identical MBR ria have been shown to be major constituents of
pilots operated in parallel. They demonstrated biofilms on building façades (Barberousse et al.,
that high PS concentrations in the sludge super- 2006a,b) causing aesthetic damage, deterioration
natant corresponded to high fouling rates. Also, of the underlying material and aiding coloniza-
the PS fraction was of microbiological origin, tion by other microorganisms (Ortega-Calvo et al.,
and the temperature and stress conditions of 1991). Also, biofilms growing on building walls
the microorganisms had an influence on the have an influence on the heat uptake of buildings,
EPS produced, i.e. increased viscosity and PS increasing the energy cost required for additional
concentration. Yun et al. (2006) also studied the air conditioning (Flemming, 2002). The biofouling
effect of dissolved oxygen on membrane filter- contributes to “abiotic” deterioration processes
ability by comparing two MBRs operated at due to the change of the material structure and
aerobic and anoxic conditions for the treatment their thermo-hygric characteristics (Sanchez-Silva
of synthetic dye wastewater. These investiga- and Rosowsky, 2008). Furthermore, mechani-
tors observed that the rate of membrane foul- cal pressure due to the shrinking and swelling of
ing for the anoxic MBR was greater than that for the biofilms may cause a further weakening of
the aerobic MBR and production of more EPS in the surface layer (Warscheid and Braams, 2000),
biofilms increased the membrane fouling in an leading to the modification of the stone’s pore
aerobic MBR. It was concluded that the rate of size and causing changes of moisture circulation
membrane fouling in the anoxic phase was more patterns and temperature response (Garty, 1991;
rapid than that in the aerobic phase, regardless Warscheid, 1996).
of EPS amount, and a greater hydraulic barrier A greater understanding of the nature of the
could have been caused by more uniform dis- polymers produced by microorganisms would
tribution of PSs in the highly spread EPS in the help development of anti-adhesive coatings for

building façade protection. Barberousse et al. grow on the surfaces of process equipment, to
(2006c), who studied the released PSs (RPSs) produce thick biofilm or “slime”. The biofilm
and CPSs secreted by algal and cyanobacte- development is often noticed within paper-
rial isolates from biofilms on building façades, machines, particularly at interfaces between such
found polymers with anionic and hydropho- a machine and water, and can account for 10–
bic properties that varied between the differ- 20% of all machine downtime (Ludensky, 2003).
ent strains. In the algal isolates, the RPSs and The slimy nature of paper mill biofilms is assign-
CPSs were mainly composed of Man, Rha and able to the presence of EPS, 90% of which is PSs
Gal; in the cyanobacterial isolates constituents (Allison, 1993). Slime deposits act as a continuous
were Glc and Gal, with Ara, xylose (Xyl) and source of contamination of circulating waters and
Fuc as minor residues (i.e. 15% of the molar the final product (Ludensky, 2003). Importantly,
composition). A significant correlation was it is essential to know the chemical composition
reported between RPS and CPS compositions of the slime deposits for optimal biofilm control
for some of the polymer extracts, thus validat- by chemical and/or enzymatic methods.
ing the hypothesis that CPSs dissolve to form Biofilm contamination is responsible for a
RPSs (Gloaguen et al., 1995). In addition, some wide range of operational problems, includ-
exopolymeric materials with multifunctional ing runnability problems with wet end-breaks,
groups may participate in metal corrosion, e.g. paper sheet defects from slime sloughing onto
be involved in adhesion of Thiobacillus albertis the circulating wire, malodours that can be car-
to elemental sulfur (Bryant et al., 1984), but also ried over onto the finished paper, etc. (Elsmore
aid in dissolving calcium from concrete, thereby et al., 1999). The main sources of microorgan-
degrading building material, especially in syn- isms in the process are the water used and the
ergy with strains of the Fusarium fungus (Gu recycled pulp, but also additives, fillers, dyes,
et al., 1998). Overall loss of concrete strength, pigments, starches and coatings can contribute,
cracking and eventual failure can result. depending on the types of paper being manufac-
In addition to biogenic transformation of tured and the mill in which they are produced
the stone surface, which comprises agglutina- (Ludensky, 2003). In addition, the paper indus-
tion of surface particles and re-mineralization, try is moving towards environmentally-friendly
extracellular PSs protect microbial cellular and processes using a closed-loop procedure of
enzyme functioning during dry and hot periods. water utilization and an increased consump-
Kemmling et al. (2004) demonstrated that, in sev- tion of recycled fibres as raw material (Blanco
eral polymers (i.e. alginate, dextran, and levan), and Gaspar, 1998). This results in an increase
a typical extracellular enzyme, the -amylase, in microbial activity and problems due to
developed enhanced resistance against desicca- microbial-related deposits (Verhoef et al., 2005).
tion stress, hence the overall stabilizing effect of PS A wide range of microorganisms is found in
preserves the biological activity of the colonizing paper manufacturing mills (Blanco et al., 1996;
organisms against repeated drying and wetting. Desjardins and Beaulieu, 2003) (Table 39.2).
According to Safade (1988), the organisms
involved in slime production and colonization
3.4. Slimes in paper production
can be divided into two groups: primary organ-
Paper manufacturing employs a warm and isms, e.g. Bacillus spp. and Sphaerotilus natans, that
nutrient-rich environment advantageous for accumulate slime and aid secondary organisms
microbial growth, with the usage of a range to grow, e.g. Klebsiella spp., Achromobacter spp.
of raw materials introducing a wide variety of and Pseudomonas spp. Filamentous bacteria, such
microorganisms into the paper mill, which can as Sphaerotilus spp., are capable of accumulating

Table 39.2 Microbial genera found in the paper-mill environment
Genera of microorganisms Reference
Bacillus, Brevundimonas, Cytophaga, Enterobacter, Klebsiella, Paenibacillus, Starkeya Rättö et al., 2005
Flavobacterium, Pseudomonas, Bacillus, Klebsiella, Sphaerotilus, Citrobacter, Burkholderia, Enterobacter Verhoef et al., 2005
Burkholderia, Alcaligenes, Bacillus Lindberg et al., 2001
Sinorhizobium, Rhizobium, Azorhizobium, -, -, -Proteobacteria, Bacteroides Lahtinen et al., 2006
Bacillus, Deinococcus, Ochrobactrum, Thermomonas Kolari et al., 2001
Flectobacillus, Cytophaga, Flavobacterium, Bacillus, Paenibacillus, Chryseobacterium, Norcardiopsis, Oppong et al., 2003
Streptomyces
Acidovorax, Acinetobacter, Aureobacterium, Bacillus, Brevibacterium, Deinococcus, Enterococcus, Väisänen et al., 1998
Xanthobacter
large amounts of slime that can clog pipes and produced in biofilms depends on the surface-
filters, bind organic and inorganic deposits, and colonizing microorganisms, the environmental
produce tenacious slimes (Pellegrin et al., 1999). conditions and the available substrate (Allison,
In particular, EPS produced by S. natans has been 1993). Thus, Lindberg et al. (2001) showed that
structurally characterized (Takeda et al., 2002). B. cepacia and Burkholderia pickettii biofilm PSs
The sheaths of that filamentous bacterium are consist mainly of Gal, Glc, Man and Rha sugar
covered with slime consisting of a gellan-like, units, but that biofilms of different strains of
acidic PS composed of pyranosidic Glc, Rha and B. cepacia have different proportions of Gal:
d-glucuronic acid (GlcA) residues forming tetras- Man:Rha. Also, it had been postulated that a
accharide repeating units: →4)--d-Glcp-(1→2)- microorganism produces only one or two differ-
-d-GlcAp-(1→2)--l-Rhap-(1→3)--l-Rhap-(1→. ent PSs and very seldom both at the same time
Takeda et al. (2002) suggested that the hygro- (Schenker et al., 1997). Importantly, Lindberg
scopic properties of the surface of the sheath of et al. (2001) observed that the change of the
S. natans, due to PS, might also be the reason for sugar composition of pure-culture biofilms
bulking of the activated sludge in wastewater depended on the composition of the medium.
treatment systems. In addition, pink-pigmented In addition, Rättö et al. (2005) observed minor
filamentous bacteria have been found in paper amounts of additional sugars in almost all
mill deposits that contribute to slime production tested PS samples from paper-machine slime,
and are responsible for the pink stains in the fin- which may reflect production of more than one
ished paper (Oppong et al., 2003). Despite rep- PS by the isolates, but it cannot be ruled out that
resenting only 10% of the total slime-producing these were impurities liberated from contami-
population, S. natans usually contributes to for- nating bacterial cells or derived from the small
mation of viscous and rubbery slime which, even amount of yeast extract in the medium.
in small amounts, causes a pink colour pigmen- According to Rättö et al. (2005), the EPS
tation in paper machines (Johnsrud, 1997). produced by slimy isolates contains hetero-
Paper-machine slime is usually a mixture polysaccharides composed of varying amounts
of microbial and chemical deposits containing of the monosaccharides Fuc, Rha, Gal, Glc,
wood fibres and other process water compo- Man and GlcA, which also have been reported
nents, in addition to the biofilm material. It is by Väisänen et al. (1994) as the main constitu-
well established that the type of EPS and PSs ents of bacterial PSs in paper-machine slimes.

Furthermore, Rättö et al. (2006) showed the Furthermore, Verhoef et al. (2005) established
presence of colanic acid produced by the entero- the chemical structure of two exopolysaccha-
bacteria isolated from the slime collected from rides that they considered were responsible for
the paper mills. The importance of colanic acid slime formation within pulp and paper manufac-
(Figure 39.1) in biofilm growth has been dem- turing and were produced by B. vesicularis and
onstrated for E. coli (Prigent-Combaret et al., Methylobacterium spp. The latter was found to
1999). Colanic acid-deficient mutants of E. coli be excreted as a highly pyruvated galactan with
form a one- or two-layer thick biofilm, but not the repeating unit: →3)-[4,6-O-(1-carboxyethyli
the usual three-dimensional complex structures dene)]- -d-Galp-(1 →3)[4,6- O -(1-carbox
(Prigent-Combaret et al., 2000; Danese et al., yethylidene)]--d-Galp-(1→3)--d-Galp-(→
2000). Thus, Danese et al. (2000) suggested that (Verhoef et al., 2003). Furthermore, B. vesicularis
colanic acid is not so much needed for establish- produces a linear exopolysaccharide without
ing biofilms, but for maintaining its architecture non-sugar substituents containing a tetrasac-
in the face of changing environmental condi- charide repeating unit: →4)--l-GlcpA-(1→4)-
tions, such as alterations in medium bulk flow. -d-GalpA-(1→4)--l-Rhap-(1→4)--d-Glcp-(1→
Of note, Kolari et al. (2001) found that (Verhoef et al., 2002).
Bacillus spp. are not primary biofilm form- In addition, Verhoef et al. (2005) studied the
ers in paper-machines but slime is responsi- sugar composition of a large number of exopoly
ble for their persistence in biofilms formed saccharide produced by bacterial strains iso-
by primary colonizers, such as Deinococcus lated from different Finnish, French and Spanish
geothermalis. Consistent with this, Rättö et al. paper mills using high performance size exclu-
(2005) observed that Bacillus cereus, originally sion chromatography and principal component
isolated from the slime of a paper-machine analysis. These investigators differentiated four
disc filter as a co-culture with Brevundimonas groups of slime-producing species: Bacillus and
vesicularis, did not produce slime itself. related genera producing EPSs with high Man
Moroever, B. vesicularis was the most efficient and/or Glc levels; Klebsiella with Gal and Rha as
PS producer and its PS was a linear polymer major sugar moieties of their EPSs; Enterobacter
with a repeating unit containing Rha, Glc, and related genera with EPS similar to colanic
GlcA and d-galacturonic acid (GalA). acid (containing the typical sugar moiety, fucose);
and EPS-producing Methylobacterium with high
3 or 6
Gal and pyruvate levels. However, in place of
β-Gal 4 Pyr time-consuming sugar composition analysis
1
↓ Verhoef et al. (2005) also discussed the potential
4 to use Fourier transform infrared spectroscopy
β-GlcA (FT-IR), as a possible tool for pattern recognition
Colanic acid 1
and clustering of exopolysaccharide structures.
↓
3
β-Gal
1
↓
OAc 4. Microbially influenced
4 corrosion (MIC)
[→3)-β-Fuc-(1→4)-α-Fuc-(1→3)-β-Glc-(1→]n
Figure 39.1 Structure of colanic acid monomer of E.

coli K-12 (Danese et al., 2000). Abbreviations: Fuc, l-fucose;
Corrosion is an electrochemical process
Gal, d-galactose; GlcA, d-glucuronic acid; Glc, d-glucose; that is described as chemical oxidation of met-
OAC, O-acetyl group; Pyr, pyruvate. als and/or their mixtures (i.e. alloys), which

4. Microbially influenced corrosion 793
involves the transfer of electrons in the pres- number of metals have been reported to cross-
ence of an electrolyte through a series of oxida- link microbial PSs (Geesey and Jang, 1989)
tion (anodic) and reduction (cathodic) reactions, with metal ions being essential for the growth
with accumulation of the corrosion products on of bacteria. Moreover, the interaction between
the surface (Beech and Gaylarde, 1999). PSs and/or EPS and metal ions, released at the
Biofilms influence the physicochemical inter- metal–liquid interface, can be regulated by the
action between a metal and its surroundings, amount of metal ion species. Hence, the colo-
causing a deterioration of the metal called bio- nization of a metal surface is dependent on the
corrosion or MIC (Beech, 2003). Importantly, availability and the type of metal ions, i.e. the
Beech et al. (2006) suggested use of the term metal species and their reactivity as determined
MIC for biofilm-influenced corrosion, as the by the metal oxidation state (Beech, 2004). For
term “biocorrosion” is used commonly to example, the heterotrophic bacteria called “acid
describe the corrosion of implant metal and streamers”, who produce slime consisting of
alloys induced by host tissue. neutral and acidic PSs and RNA (Johnson and
Most metals are colonized by microorgan- Kelso, 1981), are able to participate in oxido-
isms but this does not mean they are suscepti- reduction of iron bound within their exopoly-
ble to MIC. For example, titanium has excellent mer matrix (Johnson et al., 1993). Therefore, it
resistance against MIC, although it accumulates has been hypothesized that carboxylic groups of
biofilms (Beech et al., 2006). Overall, it has been the exopolysaccharides and phosphate groups
proposed that MIC constitutes 10–50% of all from nucleic acid degradation could bind met-
metallic corrosion, depending on the industrial als, hence increasing the overall metal-binding
field (Booth, 1964; Flemming, 1996; Coetser and capacity of EPS (Beech, 2004). This would influ-
Cloete, 2005), and causing financial losses due to ence the electrochemical behaviour of a metal
equipment biofouling and the cost requirement through the formation of metal concentration
for prevention measures. Microorganisms within cells and galvanic coupling (Ford et al., 1988).
biofilms influence the kinetics of cathodic and/or Corrosion processes and microorganisms
anodic reactions (direct), assist in the establish- involved are extensively reviewed in Beech and
ment of the electrolyte in the cell (indirect) and Gaylarde (1999), Hamilton (2003) and Coetser
modify the chemistry of the protective layers by and Cloete (2005) and here we concentrate on
acceleration or inhibition of corrosion (Beech and the MIC related to biofilms and EPS. Depending
Sunner, 2004). The bacteria associated with corro- on the characteristics of the microorganisms,
sion of cast iron, and mild and stainless steel are i.e. the aerobic and anaerobic groups (see Table
sulfate-reducing bacteria (SRB), sulfur-oxidizing 39.3), different types of corrosion reactions con-
bacteria, iron-oxidizing/reducing bacteria, man- tribute to MIC:
ganese-oxidizing bacteria and bacteria secreting
organic acids and exopolymers or slime (Table 39.3). (i) An aerobic biofilm causes corrosion by
These organisms can coexist in biofilms and are the formation of differential aeration or
able to influence electrochemical processes as a concentration cells (Ford and Mitchell,
consequence of their metabolic activity (Beech and 1990), a process called tuberculation. The
Gaylarde, 1999). most common MIC processes take place
Corrosion of a technical material in the pres- in aerobic environments. Microorganisms
ence of biofilms, the role of EPS and, in par- from various classes such as bacteria,
ticular, the role of PS in corrosion have been fungi, algae, etc., grow in a region where
reviewed in detail elsewhere (Beech, 2004; nutrients such as water and oxygen are
Beech and Sunner, 2004). In summary, a large available. The dissolution of metal (as

Table 39.3 Microbial genera involved in MIC in aerobic and anaerobic environments, as described by Beech and
Gaylarde (1999) and Coetser and Cloete (2005)
Group Genera of microorganisms
Aerobic MIC
Sulfur oxidizers Thiobacillus
Iron and manganese oxidizers Gallionella, Sphaerotilus, Crenothrix, Leptothrix, Clonothrix, Lieskeella,
Siderocapsa, Metallogenium, Pseudomicrobium
“Slime formers” Pseudomonas, Escherichia, Flavobacterium, Aerobacter, Clostridium,
Bacillus, Desulfovibrio, Desulfotomaculum
Anaerobic MIC
SRB Desulfovibrio, Desulfobulbus, Desulfotomaculum, Desulfuromonas,
Desulfobacter, Desulfosarcina, Desulfonema, Clostridium
Iron-reducing bacteria Alteromonas, Shewanella
Other hydrogenase-positive microorganisms Chlorophyta, Cyanophyta
SRB: sulfate-reducing bacteria.
metallic cations) under aerobic conditions contribute to corrosion by excessive slime

releases an excess of electrons that are production creating differential oxygen
captured by nearby cathodic sites, and concentrations and, thus, concentration
the overall reaction leads to the formation cells (Jack, 2002). In particular, sheathed
and subsequent precipitation of insoluble filamentous S. natans has been reported to
corrosion products (Sanchez-Silva and be able to oxidize iron with the oxidation
Rosowsky, 2008). Aerobic corrosion takes products deposited on the surface of the
place through the damage of an oxide sheath (van Veen et al., 1978). Nonetheless,
film or rapid pitting which occurs under Takeda et al. (2002) suggested that the
the biofilm when oxygen cannot reach the gellan-like acidic PS of S. natans is
metal surface (Borenstein, 1994). Sulfur responsible for this as the sheath itself
oxidizers may be involved, chiefly of does not contain acidic molecules.
the genus Thiobacillus that form sulfuric Finally, other aerobic bacteria, called
acid, which is a strongly corrosive agent, “slime formers”, grow on the metal surface
especially on concrete structures within and exclude oxygen via respiration;
which steel reinforcements are corroded the slime, e.g. excreted extracellular
and carbonates solubilized. Also involved PSs, impedes oxygen diffusion, thereby
are iron and manganese oxidizers causing creating an oxygen concentration cell
corrosion through production of ferric and playing a role in the aggregation of
chloride which is extremely aggressive bacteria on the surfaces, thus creating a
and pits stainless steel (Coetser and unique milieu for further development of
Cloete, 2005). In particular, Pedomicrobium microbial communities and progressive
manganicum oxidizes manganese in MIC (Coetser and Cloete, 2005). Davidson
drinking water systems and binds colloidal et al. (1996) showed that the concentration
MnO2 in the extracellular PS (Ridge of protein and carbohydrate produced by
et al., 2007). The iron-oxidizing bacteria the bacterium Acidovorax delafieldii was

5. Conclusions 795
correlated with the surface-associated (or “patchy”) with the spatial distribution
copper found in the bulk aqueous phase of the microbial species (Coetser and
(i.e. corrosion). In addition, Pseudomonas Cloete, 2005). Additionally, corrosion
spp. have been reported to be involved with different combinations of mixed
in corrosion by colonizing metal surfaces, bacterial cultures is notably higher than
thus forming thin films with corrosion that in pure cultures, indicating the
deposits on metal surfaces, thereby importance of microbial synergy (Pitonzo
creating oxygen-free environments which et al., 2004). Variability in the bacterial
harbour SRB (Iverson, 1987). species composition of a biofilm results
(ii) An anaerobic biofilm is where the in differences in metabolic activities and,
mechanism of corrosion of iron and steel thus, in similar systems under the same
is by cathodic or anodic depolarization environmental conditions corrosion
involving the removal of hydrogen by the processes can vary significantly (Beech
hydrogenase system of the microorganism. and Sunner, 2004).
From this microbial group, SRB have
been recognized as the most significant
contributor to MIC; the two main genera
involved are Desulfovibrio and Clostridium.
5. Conclusions
The MIC produced by SRB is closely
linked to the presence of biofilms that are Due to the variety of aqueous-surface inter-
held together by microbial EPS (Coetser faces being susceptible to biofouling processes,
and Cloete, 2005). In the presence of control of this fouling is a very multifarious
SRB, steel and other iron alloys in an problem and a proper understanding of the
anaerobic aqueous environment corrode dynamics, mechanisms and factors controlling
up to four times faster than during biofouling in various environments may help
oxygen-promoted corrosion. Initially, development of suitable strategies to solve the
microbial colonization starts with aerobic problem (see Research Focus Box). It is gener-
microorganisms which form biofilms ally accepted that a greater knowledge of the
with a strong reducing environment at structure and functions of the EPS, and its PS
their point of attachment where the SRB component in particular, would aid the devel-
start to proliferate (Hamilton, 1985). The opment of methods to remove and/or prevent
SRB perform dissimilatory reduction of biofilm formation. Considering the diverse envi-
sulfur compounds such as sulfate, sulfite, ronments which bacteria inhabit and the het-
thiosulfate and sulfur itself to sulfide, with erogeneous PSs produced, there can be a wide
hydrogen sulfide also being important for disparity in biofilm structure, thus analysed
the maintenance of anaerobiosis (Coetser samples may have extensive variations in com-
and Cloete, 2005). position. Hence, examining for similar struc-
(iii) An aerobic–anaerobic biofilm can tures between the subunits of the polymers that
contribute to MIC, whereby oxygen provide a functional specificity to biofilm EPS
is present but anaerobic microniches might aid development of enzymatic treatment
and/or an anaerobic layer exist. The SRB protocols. For example, it has been shown that
colonize these niches even when dissolved PS-degrading enzymes of microbial or phage
oxygen penetrates the entire biofilm at origin can cause localized destruction and pos-
other locations (Lee et al., 1995). Mixed sible weakening of the biofilm matrix structure
population biofilms are heterogeneous (Sutherland, 2001c). Also, the fast identification

of EPS structures would be advantageous for processes can vary significantly (Beech and
effective control strategies in order to define the Sunner, 2004). In addition, even if the microbial
best anti-slime approach. Thus, in place of time- composition of the biofilm is identical, alterations
consuming sugar composition analysis, Verhoef in nutrient availability can influence the biofilm
et al. (2005) have investigated the potential for PS composition significantly. Thus, long-term
use of FT-IR as a possible tool for pattern recog- biofilm community studies would aid knowl-
nition and clustering of EPS structures. edge about PS stability. In addition, good model
Another important aspect of biofouling is that systems are required to study specific biofouling
the characteristics of the surface material have environments which is a very time-consuming
an effect on the density of biofilm formation. research field as there is no universal biofouling
Even latex and other plastic surfaces have been assemblage. Every industrial sector has to focus
shown to support microbial growth and biofilm on particular microbial communities and the
formation (Rogers et al., 1994). Furthermore, the respective environmental conditions, e.g. oxy-
corrosivity of galvanized steel in an aqueous gen availability, temperature, humidity, stress,
environment results in more extensive corrosion etc., all of which affect biofilm structure, includ-
products or surface area available for microbial ing biofilm-associated PSs.
colonization. Thus, due to the rough corroded As has been shown, a biofilm is a nutrient-rich
layer, galvanized steel may provide a suitable environment, especially EPSs with a high PS con-
niche for microorganisms participating in rapid tent, although EPSs are potentially biodegradable
biofouling (Pasmore et al., 2002). (Zhang and Bishop, 2003) and may especially
Of particular note, corrosion with differ- be utilized when the microbial community is in
ent combinations of mixed bacterial cultures is a starvation state (Ceyhan and Ozdemir, 2008).
notably higher than with pure cultures, hence Therefore, the study of biofilm microbial com-
indicating the importance of microbial syn- munities could prove to be the source of possible
ergy (Pitonzo et al., 2004). Variability in bacte- anti-fouling agents. On the other hand, the intro-
rial species composition of a biofilm can result duction of beneficial microbial biofilms might
in differences in metabolic activities and, under protect against the damaging effects of biofouling,
the same environmental conditions, corrosion e.g. by passivation of a surface (Qian et al., 2007).
Research Focus
Box
l There is a need for a methodological for studying the importance of PS production,

characterization of microbial communities in are required.
connection to their environments, i.e. nutrient l Chemical structure characterization and
and oxygen availability, in which they exist analysis of biofilm PSs from different
to provide a better understanding of bacterial biofouling environments would provide
involvement in PS production. important insights.
l Good laboratory models for biofilm
formation, stability and longevity, as well as

References 797
Acknowledgements Beech, I.B., 2004. Corrosion of technical materials in the

presence of biofilms – current understanding and state-
of-the art methods of study. Int. Biodeterior. Biodegrad.
The authors gratefully acknowledge the 53, 177–183.
financial support of Griffith University, Science Beech, I.B., Gaylarde, C.C., 1999. Recent advances in the
study of biocorrosion – an overview. Rev. Microbiol. 30,
Foundation Ireland and the EU Marie Curie 177–190.
Programme (Grant No. MTKD-CT-2005-029774) Beech, I.B., Sunner, J., 2004. Biocorrosion: towards under-
for their studies. standing interactions between biofilms and metals.
Curr. Opin. Biotechnol. 15, 181–186.
Beech, I.B., Sunner, J.A., Hiraoka, K., 2005. Microbe-surface
References interactions in biofouling and biocorrosion process. Int.
Microbiol. 8, 157–168.
Al-Ahmad, M., Aleem, F.A.A., Mutiri, A., Ubaisy, A., Beech, I.B., Sunner, J.A., Arciola, C.R., Cristiani, P., 2006.
2000. Biofouling in RO membrane systems. Part 1: Microbially-influenced corrosion: damage to prostheses,
Fundamentals and control. Desalination 132, 173–179. delight for bacteria. Int. J. Artif. Organs. 29, 443–452.
Allison, D.G., 1993. Biofilm-associated exopolysaccharides. Bhaskar, P.V., Bhosle, N.B., 2005. Microbial extracellular pol-
Microbiol. Eur. 1, 16–19. ymeric substances in marine biogeochemical processes.
Ang, W.S., Lee, S., Elimelech, M., 2006. Chemical and physi- Curr. Sci. 88, 45–53.
cal aspects of cleaning of organic-fouled reverse osmosis Blanco, M.A., Gaspar, I., 1998. Microbial aspects in recycling
membranes. J. Membr. Sci. 272, 198–210. paper industry. In: Blanco, M.A., Negro, C., Tijero, J.
Assanta, M.A., Roy, D., Monpetit, D., 1998. Adhesion of (Eds.), COST E1, Paper Recycling: An introduction
Aeromonas hydrophilia to water distribution system pipes to Problems and their Solutions. Office for Official
after different contact times. J. Food Prot. 61, 1321–1329. Publications of the European Communities, Luxembourg,
Azis, P.K.A., Al-Tisan, I., Al-Daili, M., et al., 2003. Marine pp. 153–183.
macrofouling: a review of control technology in the con- Blanco, M.A., Negro, C., Gaspar, I., Tijero, J., 1996. Slime
text of an on-line experiment in the turbine condenser problems in the paper and board industry. Appl.
water box of Al-Jubail phase-I power/MSF plants. Microbiol. Biotechnol. 46, 203–208.
Desalination 154, 277–290. Booth, G.H., 1964. Sulphur bacteria in relation to corrosion.
Bahat-Samet, E., Castro-Sowinski, S., Okon, Y., 2004. J. Appl. Bacteriol. 27, 174–181.
Arabinose content of extracellular polysaccharide plays Borenstein, S.W., 1994. Microbiologically Influenced Corrosion
a role in cell aggregation of Azospirillium brasilense. Handbook. Woodhead Publishing Ltd., Cambridge.
FEMS Microbiol. Lett. 237, 195–203. Bott, T.R., 1998. Techniques for reducing the amount of
Baker, J.S., Dudley, L.Y., 1998. Biofouling in membrane biocide necessary to counteract the effects of biofilm
systems – a review. Desalination 118, 81–89. growth in cooling water systems. App. Therm. Eng. 18,
Balestrino, D., Ghigo, J.-M., Charbonnel, N., Haagensen, J.A.J., 1059–1066.
Forestier, C., 2008. The characterization of functions Branda, S.S., Vik, A., Friedman, L., Kolter, R., 2005. Biofilms:
involved in the establishment and maturation of Klebsiella the matrix revisited. Trends Microbiol. 13, 20–26.
pneumoniae in vitro biofilm reveals dual roles for surface Bryant, R.D., Costerton, J.W., Laishley, E.J., 1984. The role of
exopolysaccharides. Environ. Microbiol. 10, 685–701. Thiobacillus aibertis glycocalyx in the adhesion of cells to
Barberousse, H., Tell, G., Yéprémian, C., Couté, A., 2006a. elemental sulfur. Can. J. Microbiol. 30, 81–90.
Diversity of algae and cyanobacteria growing on build- Ceyhan, N., Ozdemir, G., 2008. Extracellular polysaccha-
ing facades in France. Algol. Stud. 120, 83–110. rides produced by cooling water tower biofilm bacteria
Barberousse, H., Lombardo, R.J., Tell, G., Couté, A., 2006b. and their possible degradation. Biofouling 24, 129–135.
Factors involved in the colonisation of building facades Chan, C.S., de Stasio, G., Welch, S.A., et al., 2004. Microbial
by algae and cyanobacteria in France. Biofouling 22, polysaccharides template assembly of nanocrystal
69–77. fibres. Science 303, 1656–1658.
Barberousse, H., Ruiz, G., Gloaguen, V., et al., 2006c. Chang, I.-S., Le Clech, P., Jefferson, B., Judd, S., 2002.
Capsular polysaccharides secreted by building facade Membrane fouling in membrane bioreactors for waste-
colonisers: characterisation and adsorption to surfaces. water treatment. J. Environ. Eng. 128, 1018–1029.
Biofouling 22, 361–370. Chang, W.S., Mortel, M., Nielsen, L., Nino de Guzman, G.,
Beech, I.B., 2003. Sulfate-reducing bacteria in biofilms on Li, X., Halverson, L.J., 2007. Alginate production by
metallic materials and corrosion. Microbiol. Today 30, Pseudomonas putida creates a hydrated microenviron-
115–117. ment and contributes to biofilm architecture and stress

tolerance under water-limiting conditions. J. Bacteriol. microbial products, and natural organic matter impact
189, 8290–8299. on nanofiltration membranes flux decline. Environ. Sci.
Chen, C.-L., Liu, W.-T., Chong, M.-L., et al., 2004. Technol. 41, 2491–2497.
Community structure of microbial biofilms associated Ford, T., Mitchell, R., 1990. The ecology of microbial corro-
with membrane-based water purification processes as sion. Adv. Microb. Ecol. 11, 231–262.
revealed using a polyphasic approach. Appl. Miocrobiol. Ford, T.E., Maki, J.S., Mitchell, R., 1988. Involvement of
Biotechnol. 63, 466–473. bacterial exopolymers in biodeterioration of metals.
Cheryan, M., 1998. Ultrafiltration and Microfiltration In: Houghton, D.R., Smith, R.N., Eggins, H.O.W. (Eds.),
Handbook. CRC Press-Taylor & Francis, Boca Raton. Biodeterioration 7, Proceedings of the Seventh Inter
Coetser, S.E., Cloete, T.E., 2005. Biofouling and biocorrosion in national Biodeterioration Symposium. Elsevier Applied
industrial water systems. Crit. Rev. Microbiol. 31, 213–232. Science, Barking, Essex, pp. 378–384.
Danese, P.N., Pratt, L.A., Kolter, R., 2000. Exopolysaccharide Garcia-Fulgueiras, A., Navarro, C., Fenoll, D., Garcia, J.,
production is required for development of Escherichia coli González-Diego, P., Jiménez-Buñuales, T., 2003.
K-12 biofilm architecture. J. Bacteriol. 182, 3593–3596. Legionnaires’ disease outbreak in Murcia, Spain.
Darby, C., Hsu, J.W., Ghori, N., Falkow, S., 2002. Emerging Infect. Dis. 9, 915–921.
Caenorhabditis elegans: plague biofilm block food intake. Garty, J., 1991. Influence of epilithic microorganisms on the
Nature 417, 243–244. surface temperature of building walls. Can. J. Bot. 68,
Davidson, D., Beheshti, B., Mittelman, M.W., 1996. Effects of 1349–1353.
Arthrobacter sp., Acidovorax delafieldii and Bacillus megath- Gaylarde, C., Ribas Silva, M., Warscheid, Th., 2003.
erium colonization on copper solvency in a laboratory Microbial impact on building materials: an overview.
reactor. Biofouling 9, 279–292. Mater. Struct. 36, 342–352.
Desjardins, E., Beaulieu, C., 2003. Identification of bacteria Geesey, G.G., Jang, L., 1989. Extracellular polymers for metal
contaminating pulp and a paper machine in a Canadian binding. In: Beveridge, T.J., Doyle, R.J. (Eds.), Bacterial
paper mill. J. Ind. Microbiol. Biotechnol. 30, 141–145. Interactions with Metallic Ions. Wiley, New York,
Dondero, T.J., Rendtorff, R.C., Maluson, G.F., et al., 1980. pp. 223–247.
An outbreak of legionnaires’ disease associated with a Gloaguen, V., Morvan, H., Hoffmann, L., 1995. Released and
contaminated air-conditioning cooling tower. N. Engl. J. capsular polysaccharides of Oscillatoriaceae (Cyanophyceae,
Med. 302, 365–370. Cyanobacteria). Algol. Stud. 78, 53–69.
Donlan, R.M., 2001. Biofilms and Device-Associated Götz, F., 2002. Staphylococcus and biofilms. Mol. Microbiol.
Infections. Emerg. Infect. Dis. 7, 277–281. 43, 1367–1378.
Donlan, R.M., 2002. Biofilms: microbial life on surfaces. Gu, J.-D., Ford, T.E., Berke, N.S., Mitchell, R., 1998.
Emerging Infect. Dis. 8, 881–890. Biodeterioration of concrete by the fungus Fusarium. Int.
Eiff, C.V., Jansen, B., Kohnen, W., Becker, K., 2005. Infections Biodeterior. Biodegrad. 41, 101–109.
associated with medical devices. Drugs 65, 179–214. Habash, M., Reid, G., 1999. Microbial biofilms: their devel-
Elsmore, R., Gilbert, P., Ludensky, M., Coulburn, J., 1999. opment and significance for medical device-related
Biofilms in paper manufacturing. In: Wimpenny, G., infections. J. Clin. Pharmacol. 39, 887–898.
Walker, B. (Eds.), Biofilms: The Good, the Bad and the Haberkamp, J., Ernst, M., Böckelmann, U., Ulrich Szewzyk,
Ugly. Bioline, Cardiff, pp. 81–89. U., Jekel, M., 2008. Complexity of ultrafiltration mem-
Flemming, H.-C., 1996. Biofouling and microbiologically brane fouling caused by macromolecular dissolved
influenced corrosion (MIC) – an economical and techni- organic compounds in secondary effluents. Water Res.
cal overview. In: Heitz, E., Sand, W., Flemming, H.-C. 42, 3153–3161.
(Eds.), Microbial Deterioration of Materials. Springer- Hall-Stoodley, L., Costerton, J.W., Stoodley, P., 2004. Bacterial
Verlag, Heidelberg, pp. 5–14. biofilms: from the natural environment to infectious dis-
Flemming, H.-C., 2002. Biofouling in water systems – eases. Nat. Rev. 2, 95–108.
cases, causes and countermeasures. Appl. Microbiol. Hamilton, W.A., 1985. Sulphate-reducing bacteria and
Biotechnol. 59, 629–640. anaerobic corrosion. Ann. Rev. Microbiol. 39, 195–217.
Flemming, H.-C., Wingender, J., 2001. Relevance of microbial Hamilton, W.A., 2003. Microbially influenced corrosion as a
extracellular polymeric substances (EPSs) – part I: struc- model system for the study of metal microbe interactions:
tural and ecological aspects. Water Sci. Technol. 43, 1–8. a unifying electron transfer hypothesis. Biofouling 19,
Flemming, H.-C., Schaule, G., Griebe, T., Schmitt, J., 165–176.
Tamachkiarowa, A., 1997. Biofouling – the Achilles heel Harris, A., 2000. Problems associated with biofilms in cool-
of membrane processes. Desalination 113, 215–225. ing tower systems. In: Keevil, C.V., Godfree, A., Holt, D.,
Fonseca, A.C., Summers, R.S., Greenberg, A.R., Hernandez, Dow, C. (Eds.), Biofilms in the Aquatic Environment.
M.T., 2007. Extra-cellular polysaccharides, soluble Springer, Berlin, pp. 139–144.

REFERENCES 799
Herzberg, M., Elimelech, M., 2007. Biofouling of reverse Lee, W., Lewandowski, Z., Nielsen, P.H., Hamilton, W.A.,
osmosis membranes: role of biofilm-enchanced osmotic 1995. Role of sulfate-reducing bacteria in corrosion of
pressure. J. Membr. Sci. 295, 11–20. mild steel: a review. Biofouling 8, 165–194.
Iverson, W.P., 1987. Microbial corrosion of metals. Adv. Lindberg, L.E., Holmbom, B.R., Väisänen, O.M., Weber,
Appl. Microbiol. 32, 1–36. A.M.-L., Salkinoja-Salonen, M.S., 2001. Sugar composi-
Ivnitsky, H., Katz, I., Minz, D., et al., 2007. Bacterial com- tion of biofilms produced by paper mill bacteria. Appl.
munity composition and structure of biofilms develop- Microbiol. Biotechnol. 55, 638–643.
ing on nanofiltration membranes applied to wastewater Ludensky, M., 2003. Control and monitoring of biofilms in
treatment. Water Res. 41, 3924–3935. industrial applications. Int. Biodeterior. Biodegrad. 51,
Jack, T.R., 2002. Biological corrosion failures. ASM 255–263.
Handbook Volume 11: Failure Analysis and Prevention. Majumdar, I., D’Souza, F., Bhosle, N.B., 1999. Microbial
ASM International, Materials Park, Ohio. exopolysaccharides: effect on corrosion and partial
Jain, A., Bhosle, N.B., 2008. Role of β-(1→4)-linked polymers chemical characterization. J. Indian Inst. Sci. 79, 539–550.
in the biofilm structure of marine Pseudomonas sp. CE-2 Maruthamuthu, S., Muthukumar, N., Natesan, M.,
on 304 stainless steel coupons. Biofouling 24, 283–290. Palaniswamy, N., 2008. Role of air microbes on atmos-
Johnson, D.B., Kelso, W.I., 1981. Extracellular polymers of pheric corrosion. Curr. Sci. 94, 359–363.
acid streamers from pyritic mines. Environ. Pollut. Ser. Michael, L., 2003. Control and monitoring of biofilms in
24, 291–301. industrial applications. Int. Biodeterior. Biodegrad. 51,
Johnson, D.B., Ghauri, M.A., McGinness, S., 1993. 255–363.
Biogeochemical cycling of iron and sulphur in leaching Molino, P.J., Wetherbee, R., 2008. The biology of biofouling
environments. FEMS Microbiol. Rev. 11, 63–70. diatoms and their role in the development of microbial
Johnsrud, S.C., 1997. Biotechnology for solving slime prob- slimes. Biofouling 24, 365–379.
lems in the pulp and paper industry. In: Scherper, P. Mopper, K., Schultz, C., Chevolot, L., Germain, C., Revuelta,
(Ed.), Advances in Biochemical Engineering/ R., Dawson, R., 1991. Determination of sugars in uncon-
Biotechnology. Springer-Verlag, Heidelberg, pp. 311–328. centrated seawater and other natural waters by liquid
Judd, S., 2006. The MBR Book: Principles and Applications chromatography and pulsed amperometric detection.
of Membrane Bioreactors in Water and Wastewater Environ. Sci. Technol. 26, 133–149.
Treatment. Elsevier, Oxford. Moran, A.P., Annuk, H., 2003. Recent advances in under-
Kaplan, J.B., Velliyagounder, K., Ragunath, C., Rohde, H., standing biofilms of mucosae. Rev. Environ. Biotechnol.
Mack, D., Knobloch, J.K., 2004. Genes involved in the 2, 121–140.
synthesis and degradation of matrix polysaccharide in Moran, A.P., Ljungh, Å., 2003. Physico-chemical properties of
Actinobacillus actinomycetemcomitans and Actinobacillus extracellular polymeric substances. In: Lens, P., Moran,
pleuropneumoniae biofilms. J. Bacteriol. 186, 8213–8220. A.P., O’Mahony, T., Stoodley, P., O’Flaherty, V. (Eds.),
Kemmling, A., Kämper, M., Flies, C., Schieweck, O., Biofilms in Medicine, Industry and Environmental
Hoppert, M., 2004. Biofilms and extracellular matrices Biotechnology – Characteristics, Analysis and Control.
on geomaterials. Environ. Geol. 46, 429–435. IWA Publishing, London, pp. 91–112.
Kim, H.Y., Yeon, K.-M., Lee, Ch.-H., Lee, S., Swaminathan, T., Mulder, M., 1996. Basic Principles of Membrane Technology.
2006. Biofilm structure and extracellular polymeric sub- Kluwer Academic Publishers, Dordrecht.
stances in low and high dissolved oxygen membrane Murphy, A.P., Moody, C.D., Riley, R.L., Lin, S.W.,
bioreactors. Sep. Sci. Technol. 41, 1213–1230. Murugaverl, B., Rusin, P., 2001. Microbiological damage
Kinzler, K., Gehrke, T., Telegdi, J., Sand, W., 2003. Bioleaching – of cellulose acetate RO membranes. J. Membr. Sci. 193,
a result of interfacial processes caused by extracellu- 111–121.
lar polymeric substances (EPS). Hydrometallurgy 71, Nichols, P.D., Nichols, C.A.M., 2008. Microbial signature
83–88. lipid profiling and exopolysaccharides: experience initi-
Kolari, M., Nuutinen, J., Salkinoja-Salonen, M.S., 2001. ated with professor David C White and transported to
Mechanisms of biofilm formation in paper machine by Tasmania. Australia. J. Microbiol. Methods. 74, 33–46.
Bacillus species: the role of Deinococcus geothermalis. J. Nivens, D.E., Ohman, D.E., Williams, J., Franklin, M.J., 2001.
Ind. Microbiol. Biotechnol. 27, 343–351. Role of alginate and its O acetylation in formation of
Kumar, C.G., Takagi, H., 1999. Microbial alkali proteases: Pseudomonas aeruginosa microcolonies and biofilms. J.
from a bioindustrial viewpoint. Biotechnol. Adv. 17, Bacteriol. 183, 1047–1057.
561–594. Nygård, K., Werner-Johansen, Ø., Rønsen, S., et al., 2008.
Lahtinen, T., Kosonen, M., Tiirola, M., Vuento, M., Oker-Blom, C., An outbreak of Legionnaires disease caused by long-
2006. Diversity of bacteria contaminanting paper machines. distance spread from an industrial air scrubber in
J. Ind. Microbiol. Biotechnol. 33, 734–740. Sarpsborg, Norway. Clin. Infect. Dis. 46, 61–69.
IV. BIOLOGICAL RELEVANCE OF MICROBIAL GLYCOSYLATED COMPONENTS

Oppong, D., King, V.M., Bowen, J.A., 2003. Isolation and enterobacteria isolated from paper machine slimes. J.
characterisation of filamentous bacteria from paper mill Ind. Microbiol. Biotechnol. 33, 359–367.
slimes. Int. Biodeterior. Biodegrad. 52, 53–62. Ridge, J.P., Lin, M., Larsen, E.I., Fegan, M., McEwan, A.G.,
Ortega-Calvo, J.J., Hernandez-Marine, M., Saiz-Jimenez, C., Sly, L.I., 2007. A multicopper oxidase is essential for man-
1991. Biodeterioration of building materials by cyano- ganese oxidation and laccase-like activity in Pedimicrobium
bacteria and algae. Int. Biodeterior. 28, 165–185. sp. ACM 3067. Environ. Microbiol. 9, 944–953.
Pasmore, M., Todd, P., Pfeifer, B., Rhodes, M., Bowman, C.N., Ridgway, H., Flemming, H.-C., 1996. Membrane biofouling.
2002. Effect of polymer surface properties on the reversi- In: Mallevialle, J., Odendal, P.E., Wiesner, M.R. (Eds.),
bility of attachment of Pseudomonas aeruginosa in the early Water Treatment: Membrane Processes. McGraw-Hill,
stages of biofilm development. Biofouling 18, 65–71. New York, pp. 6.1–6.61.
Passow, U., 2002. Transparent exopolymer particles (TEP) in Ridgway, H.F., Kelly, A., Justice, C., Olson, B.H., 1983.
aquatic environments. Prog. Oceanogr. 55, 287–333. Microbial fouling of reverse-osmosis membranes used
Patching, J.W., Fleming, G.T.A., 2003. Industrial biofilms: for- in advanced wastewater treatment technology: chemi-
mation, problems and control. In: Lens, P., Moran, A.P., cal, bacteriological, and ultrastructural analyses. Appl.
Mahony, T., Stoodley, P., O’Flaherty, V. (Eds.), Biofilms in Environ. Microbiol. 45, 1066–1084.
Medicine, Industry and Environmental Biotechnology – Rogers, J., Dowsett, A.B., Dennis, P.J., Lee, J.V., Keevil, C.
Characteristics, Analysis and Control. IWA Publishing, W., 1994. Influence of temperature and plumbing mate-
London, pp. 568–590. rial on biofilm formation and growth of Legionella pneu-
Paul, D., Abanmy, A.R.M., 1990. Reverse osmosis membrane mophila in a model potable water system containing
fouling – the final frontier. Ultra Pure Water 7, 25–36. complex microbial flora. Appl. Environ. Microbiol. 60,
Pellegrin, V., Juretschko, S., Wagner, M., Cottenceau, G., 1585–1592.
1999. Morphological and biochemical properties of Rosberg, R., 1997. Ultrafiltration (new technology), a viable
Sphaerotilus sp. isolated from paper mill slimes. Appl. cost-saving pretreatment for reverse osmosis and nano-
Environ. Microbiol. 65, 156–162. filtration – a new approach to reduce cost. Desalination
Pitonzo, B.J., Castro, P., Amy, P.S., Southam, G., Jones, D.A., 110, 107–113.
Ringelberg, D., 2004. Microbiologically influenced Rosenberger, S., Laabs, C., Lesjean, B., et al., 2006. Impact
corrosion capability of bacteria isolated from Yucca of colloidal and soluble organic material on membrane
Mountain. Corrosion 60, 64–74. performance in membrane bioreactors for municipal
Prigent-Combaret, C., Vidal, O., Dorel, C., Lejeune, P., 1999. wastewater treatment. Water Res. 40, 710–720.
Abiotic surface sensing and biofilm-dependent regula- Ruijssenaars, H.J., De Bond, J.A.M., Hartmans, S., 1999. A
tion of gene expression in Escherichia coli. J. Bacteriol. pyruvated mannose-specific xanthan lyase involved in
181, 5993–6002. xanthan degradation by Paenibacillus alginolyticus XL-1.
Prigent-Combaret, C., Prensier, G., Le Thi, T.T., Vidal, O., Appl. Environ. Microbiol. 65, 2446–2452.
Lejeune, P., Dorel, C., 2000. Developmental pathway Sadovskaya, I., Vinogradov, E., Flahaut, S., Kogan, G.,
for biofilm formation in curli-producing Escherichia coli Jabbouri, S., 2005. Extracellular carbohydrate-contain-
strains: role of flagella, curli and colanic acid. Environ. ing polymers of a model biofilm-producing strain,
Microbiol. 2, 450–464. Staphylococcus epidermidis RP62A. Infect. Immun. 73,
Prince, E.L., Muir, A.V.G., Thomas, W.M., Stollard, R.J., 3007–3017.
Sampson, M., Lewis, J.A., 2002. An evaluation of the Safade, T.L., 1988. Tackling the slime problem in a paper-
efficacy of Aqualox cooling tower systems. J. Hosp. mill. Pap. Technol. Ind. September, 280–285.
Infect. 52, 243–249. Sanchez-Silva, M., Rosowsky, D.V., 2008. biodeterioration of
Qian, P.-Y., Lau, S., Dahms, H.-U., Dobretsov, S., Harder, T., construction materials: state of the art and future chal-
2007. Marine biofilms as mediators of colonization by lenges. J. Mater. Civ. Eng. 20, 352–365.
marine macroorganisms: implications for antifouling Schaefer, A., Fane, A.G., Waite, T.D. (Eds.), 2004.
and aquaculture. Mar. Biotechnol. 9, 399–410. Nanofiltration: Principles and Applications. Elsevier
Rättö, M., Mustranta, A., Siika-aho, M., 2001. Strains degrad- Advanced Technology Books, Amsterdam.
ing polysaccharides produced by bacteria from paper Schenker, A., Popp, G., Papier, G., Schwalbach, E., 1997.
machines. Appl. Microbiol. Biotechnol. 57, 182–185. Enzyme additions for biofilm control in PM circuits.
Rättö, M., Suihko, M.-L., Siika-aho, M., 2005. Polysaccharide- Wochenbl. Papierfabr. 125, 702–709.
producing bacteria isolated from paper machine slime Solano, C.B., Garcia, J., Valle, C., Berasain, J.M., Ghigo, C.,
deposits. J. Ind. Microbiol. Biotechnol. 32, 109–114. Gamazo Lasa, I., 2002. Genetic analysis of Salmonella
Rättö, M., Verhoef, R., Suihko, M.-L., et al., 2006. Colanic enteritidis biofilm formation: critical role of cellulose.
acid is an exopolysaccharide common to many Mol. Microbiol. 43, 793–808.

References 801
Spiers, A.J., Kahn, S.G., Bohannon, J., Travisano, M., Rainey, of slime producing Brevundimonas vesicularis sp. isolated
P.B., 2002. Adaptive divergence in experimental popula- from a paper machine. Carbohydr. Res. 337, 1821–1831.
tions of Pseudomonas fluorescens. I. Genetic and phenotypic Verhoef, R., Waard de, P., Schols, H.A., Siika-aho, M.,
bases of wrinkly spreader fitness. Genetics 161, 33–46. Voragen, A.G.J., 2003. Methylobacterium sp. isolated
Sutherland, I.W., 2001a. Biofilm exopolysaccharides: a from a Finnish paper machine produces highly pyru-
strong and sticky framework. Microbiology 147, 3–9. vated galactan exopolysaccharide. Carbohydr. Res. 338,
Sutherland, I.W., 2001b. Exopolysaccharides in biofilms, flocs 1851–1859.
and related structures. Water Sci. Technol. 43, 77–86. Verhoef, R., Schols, H.A., Blanco, A., et al., 2005. Sugar
Sutherland, I.W., 2001c. The biofilm matrix – an immo- composition and FT-IR analysis of exopolysaccharides
bilized but dynamic microbial environment. Trends produced by microbial isolates from paper mill slime
Microbiol. 9, 222–227. deposits. Biotechnol. Bioeng. 91, 91–105.
Takeda, M., Nomoto, S., Koizumi, J., 2002. Structural analysis Vrouwenvelder, H.S., Paassen, J.A.M.v., Folmer, H.C.,
of the extracellular polysaccharide produced by Nederlof, J.A.M.H., Kooij, D.v.d., 1998. Biofouling of
Sphaerotilus natans. Biosci. Biotechnol. Biochem. 66, membranes for drinking water production. Desalination.
1546–1551. 118, 157–166.
Tamilvanan, S., Venkateshan, N., Ludwig, A., 2008. The Warscheid, Th., 1996. Biodeterioration of stones: analysis,
potential of lipid- and polymer-based drug delivery car- quantication and evaluation. In: Proceedings of the
riers for eradicating biofilm consortia on device-related 10th International Biodeterioration and Biodegradation
nosocomial infections. J. Control. Release 128, 2–22. Symposium, Dechema-Monograph No. 133. Dechema,
Tanji, Y., Nishihara, T., Miyanaga, K., 2007. Monitoring of Frankfurt, pp. 115–120.
biofilm in cooling water system by measuring lactic acid Warscheid, Th., Braams, J., 2000. Biodeterioration of stone: a
consumption rate. Biochem. Eng. J. 35, 81–86. review. Int. Biodeterior. Biodegrad. 46, 343–368.
Tsang, P.H., Li, G., Brun, Y.V., Freund, L.B., Tang, J.X., 2006. Wotton, R., 2004. The essential role of exopolymers (EPS) in
Adhesion of single bacterial cells in the micronewton aquatic systems. Oceanogr. Mar. Biol. Annu. Rev. 42, 57–94.
range. Proc. Natl. Acad. Sci. 103, 5764–5768. Ye, Y., Le Chlech, P., Chen, V., Fane, A.G., 2005. Evolution
Türetgen, I., Cotuk, A., 2007. Monitoring of biofilm-associated of fouling during crossflow filtration of model EPS solu-
Legionella pneumophilia on different substrata in model tions. J. Membr. Sci. 264, 190–199.
cooling tower system. Environ. Monit. Assess. 125, Yun, M.-A., Yeon, K.-M., Park, J.-S., Lee, Ch.-H., Chun, J.,
271–279. Lim, D.J., 2006. Characterization of biofilm structure
Väisänen, O.M., Nurmiaho-Lassila, E.-L., Marmo, S.A., and its effect on membrane permeability in MBR for dye
Salkinoja-Salonen, M.S., 1994. Structure and composi- wastewater treatment. Water Res. 40, 45–52.
tion of biological slimes on paper and board machines. Zhang, X., Bishop, P., 2003. Biodegradability of biofilm extra-
Appl. Environ. Microbiol 60, 641–653. cellular polymeric substances. Chemosphere 50, 63–69.
Väisänen, O.M., Weber, A., Bennasar, A., Rainey, F.A., Busse, Zhou, J., Mopper, K., Passow, U., 1998. The role of surface-
H.-J., Salkinoja-Salonen, M.S., 1998. Microbial commu- active carbohydrates in the formation of transparent
nities of printing paper machines. J. Appl. Microbiol. 84, exopolymer particles by bubble adsorption of seawater.
1069–1084. Limnol. Oceanogr. 43, 1860–1871.
van Veen, W.L., Mulder, E.G., Deinema, M.H., 1978. The Zogaj, X., Nimtz, M., Rohde, M., Bokranj, W., Romling,
Sphaerotilus-Leptothrix group of bacteria. Microbiol. U., 2001. The multicellular morphotypes of Salmonella
Rev. 42, 329–356. typhimurium and E. coli produce cellulose as the second
Verhoef, R., Waard de, P., Schols, H.A., Rättö, M., Siika-aho, M., component of the extracellular matrix. Mol. Microbiol.
Voragen, A.G.J., 2002. Structural elucidation of the EPS 39, 1452–1463.

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Summary Keywords: Biofilms; Capsular polysaccharides;

Microbial Glycobiology 781 © 2009

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

of akaganeite (-FeOOH) pseudo-single crys- aureus and S. epidermidis, respectively (Danese

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

Table 39.1 Genera of microorganisms found in different industrial environments

Environment Genera of microorganisms Reference

3.2. Biofouling in membrane-related molecules and can be applied for pretreatment

IV. Biological relevance of microbial glycosylated components

process like microfiltration or ultrafiltration periods of shutdown or storage, primarily

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

Table 39.2 Microbial genera found in the paper-mill environment

Genera of microorganisms Reference

IV. Biological relevance of microbial glycosylated components

Figure 39.1 Structure of colanic acid monomer of E.

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

Group Genera of microorganisms

SRB: sulfate-reducing bacteria.

metallic cations) under aerobic conditions contribute to corrosion by excessive slime

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

l There is a need for a methodological for studying the importance of PS production,

IV. Biological relevance of microbial glycosylated components

Acknowledgements Beech, I.B., 2004. Corrosion of technical materials in the

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

IV. BIOLOGICAL RELEVANCE OF MICROBIAL GLYCOSYLATED COMPONENTS

IV. Biological relevance of microbial glycosylated components

IV. Biological relevance of microbial glycosylated components

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