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					                                        International Biodeterioration & Biodegradation (1994) 203-221
                                                            Copyright © 1995 Elsevier Science Limited
                                                           Printed in Great Britain. All rights reserved
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ELSEVIER                      0964-8305(94)00017-8



            B i o f i l m s in B i o d e t e r i o r a t i o n - -   a Review



                      L. H. G. M o r t o n & S. B. S u r m a n
Department of Applied Biology, University of Central Lancashire, Preston, Lancashire,
                                 PR1 2HE, UK




                                        ABSTRACT

   This review defines the various types of biodeterioration processes and
   discusses the role that microbial films play in the biodeterioration of a
   number of materials of economic importance. A review of the way in which
   biofilms may form and attach to surfaces is presented and the occurrence
   and nature of biofilms is considered.
      Included in this review is an account of biodeterioration problems asso-
   ciated with water distribution systems, biocorrosion, plastics, hydrocarbons,
   paints and coatings and buildings and monuments. The micro-organisms
   involved include bacteria,fungi and algae, whiehform members of the biofilm
   communities responsiblefor the biodeterioration problems described.



                                  INTRODUCTION

Biodeterioration m a y be defined as the 'Study of the deterioration of
materials o f economic importance by micro-organisms' (Huek, 1965).
Biodeterioration is due to any undesirable change in the properties of a
material caused by the vital activities of organisms. It can be described as
the net loss in value o f a product o f natural or manufactured origin;
examples of biodeterioration can be found in both domestic and industrial
situations. The processes involved in biodeterioration have been classified
as follows:
  (1) Mechanical processes, where the material is damaged as a direct
      result of the activity of an organism, such as its movement or

                                              203
204                          L. H. G. Morton, S. B. Surman

      growth. An example of this form of biodeterioration is the damage
      caused to cabling as a result of insect or rodent attack.
  (2) Chemical assimilatory biodeterioration, perhaps the most c o m m o n
      form of biodeterioration. It occurs when a material is degraded for
      its nutritive value. The breakdown of cellulosic materials by cellu-
      lolytic micro-organisms, is an example of this type of biodeteriora-
      tion.
  (3) Chemical dissimilatory biodeterioration, which occurs when meta-
      bolic products damage a material by causing corrosion, pigmenta-
      tion, or by the release of toxic metabolites into a substance. The
      poisoning of grain by mycotoxins is an example of this process.
  (4) Soiling/biofouling, the form of biodeterioration which occurs when
      the mere presence of an organism or its excrement renders the
      product unacceptable. The biofouling of ships' hulls, the formation
      of slime in fuel lines and corrosion within water pipelines are
      examples of this form of biodeterioration.
  Microbial biodeterioration may be defined as the deterioration of
materials by micro-organisms. Microbial hydrolytic enzymes often play an
important role in these decay processes.


                                    BIOFILMS

The term 'biofilm' in the context of biodeterioration gives rise to a number
of fundamental questions:
   (i)     What are biofilms?
   (ii)    How are they formed?
   (iii)   Where are they found?
   (iv)    What is their role in biodeterioration?

W h a t is a biofilm?

Microbial biofilms are extremely complex microbial ecosystems that are
difficult to study by conventional microbiological techniques. They may
consist of complex consortia of bacteria, algae, and grazing protozoa
which may display morphological features not usually associated with the
organisms when grown in pure culture. It is therefore acknowledged to be
very difficult to produce a biofilm which is truly representative of that
found in a particular environment. The diversity of the biofilm microflora
and microfauna and their interspatial relationships are extremely difficult
to reproduce.
                            Biofilms in biodeterioration                  205

Biofilm formation

Hamilton and Characklis (1989) described the phases of biofilm develop-
ment as follows:
  (l)   the transport of organic molecules and cells to the surface,
  (2)   the adsorption of organic molecules to give a 'conditioned' surface,
  (3)   the adsorption of cells to the conditioned surface,
  (4)   the growth of adsorbed cells with associated synthesis of expoly-
        meric substances (EPS).

   Colonisation is one of the first steps leading to the subsequent forma-
tion of a biofilm on a material, resulting at best in a reduction of its
performance and, at worst, in its destruction. Colonisation is the process
by which micro-organisms adhere to surfaces. They do so by means of
extracellular polysaccharide substances, EPS, secreted by the cells. This
EPS is also called the glycocalyx. In recent years it has become apparent
that in the natural and industrial environments, bacterial adhesion is
mediated by the glycocalyx. This is a hydrated polyanionic polysaccharide
matrix produced by polymerases affixed to the lipopolysaccharide
component of the cell wall (Costerton et al., 1981, 1985). In aqueous
environments bacteria with the ability to generate glycocalyces abound.
Several factors contribute to the preferential selection of such micro-
organisms in these environments:

  • Organic and inorganic nutrients are concentrated at the solid-liquid
    interface; organisms able to secure themselves in this niche are clearly
    at an advantage (Costerton et al., 1981).
  • The glycocalyx acts as an ionic exchange matrix, trapping nutrients
    that are then transported into the cell by highly efficient permeases
    (Costerton & Geesey, 1979).
  • The glycocalyx conserves and concentrates the digestive enzymes
    released by the bacteria, thus increasing the metabolic efficiency of the
    cells (Costerton et al., 1978).
  • The glycocalyx constitutes a physical barrier that affords partial
    protection from antibacterial agents. (Costerton et al., 1981).

Where are biofilms found?

Surface associated microbial activity and colonisation, or biofilm forma-
tion is a p h e n o m e n o n that occurs in both natural and man-made envir-
onments, even in nutrient limited conditions. Biofilms may exist as
beneficial epilithic communities in rivers and streams. They are also found
206                      L. H. G. Morton, S. B. Surman

in waste water treatment plants on trickling filter beds and in the alimen-
tary canal of mammals (Costerton et al., 1986; Bryers & Characklis, 1982).
Biofilm are truly ubiquitous.

What is their role in biodeterioration?

In many industries the formation of biofilms within pipework, cooling
systems, heat exchangers and filters can cause problems. The resulting
losses of efficiency due to increased frictional resistance in pipes (McCoy
et al., 1981) or decrease in heat exchange capabilities (Trulear & Char-
acklis, 1982; Shariff & Hassa, 1985) can result in decreased production
rates and increased costs.
   Biofilms, however, are not confined to solid/liquid interfaces, they can
also be found at solid/air interfaces. Airborne pathogens and deteriogens
have been shown to be important factors in the biodeterioration of surface
coatings. Microorganisms such as algae and fungi (rather than bacteria)
often play the major role (Lloyd, 1987). Biofilms found at liquid/liquid
interfaces are implicated in hydrocarbon degradation, which includes fuel
oils and industrial coolants.
   Relationships exist between humans and biofilm micro-organisms; for
example, in the gut and in the female urethra; these relationships are often
symbiotic (Geesey et al., 1992). However, biofilms can also be detrimental
to humans, for example, when occurring as dental plaque on teeth and
dentures causing human caries and gum disease (Keevil et al., 1987).
Biofilms also occur on medical prostheses, including pacemakers,
replacement joints and indwelling catheters where colonisation causes
chronic infections in the surrounding tissue. Often these tissues tend to be
resistant to broad spectrum antimicrobial drugs and this can lead to
septicaemia. In many cases the removal of the infected prostheses is
required to prevent recurrent life-threatening infections. Biofilm forma-
tion has also been implicated in gallstone formation and in the plugging of
biliary stents used in the treatment of biliary cancer (Sung et al., 1992).

Water distribution systems

The occurrence of biofilms within domestic and industrial water distribu-
tion systems is well documented (Costerton et al., 1987; Le Chevallier
et al., 1988; Colbourne et al., 1988). Sloughing and erosion of the biofilm
surface results in an increase in planktonic micro-organisms which may
include potential human pathogens e.g. Legionella pneumophila (Alary &
Joly, 1991; van der Wende, 1988; Rowbotham, 1980; Keevil et al., 1989),
Cryptosporidia and Gardia spp. (Reasoner, 1988).
                          Biofilms in biodeterioration                   207

  Legionella pneurnophila, the main aetiological agent responsible for
Legionnaires' disease, is a micro-organism which is widespread within the
environment. It is an opportunistic human pathogen found in high
numbers in both natural and man-made aquatic environments (Grimes,
1991). Sources of infection have been found to include hot water systems,
especially in large institutions such as hospitals (Hsu et al., 1984; Stout
et al., 1992; Bezanson et al., 1992), cooling towers and evaporative
condensors (Tobin et al., 1981; Breiman, 1993; Bentham, 1993), fountains,
machine cutting coolant, misting devices, spa baths (Anon., 1991) and
nebulisers (Agrawal et al., 1991). Factors which predispose artificial man-
made environments to infection with L. pneumophila include: the
temperature of the system, stagnation which often occurs in the dead ends
of the distribution system pipework and in storage tanks (Verissimo et al.,
1990), and the presence of certain nutritional sources. These may include
the material of the system itself, scale, sediments and non-legionellaceae
micro-organisms (Anand et al., 1984; Barbaree et al., 1986; Vickers et al.,
1987; Anon., 1991; Nahapetian et al., 1991; Lfick et al., 1991; Stout et al.,
1985, 1992; Rogers et al., 1993; Breiman et aL, 1993). The presence of
other micro-organisms in the system is important. Legionella pneumophila
appears to be capable of thriving with many different micro-organisms.
The association of Legionella pneumophila with different species isolated
from aquatic sources is well documented. These include protozoa, cyano-
bacteria, algae and other bacteria (Rowbotham, 1980; Tison et al., 1980;
Tesh & Miller, 1981; Fliermans et al., 1981; Bohach & Snyder, 1983;
Wadowsky & Yee, 1983, 1985; Grimes, 1991; Pope et al., 1982; Hume &
Hann, 1984). Biofilms in man-made aquatic environments therefore
provide ecological niches ideally suited to Legionella pneumophila survival
and growth.
   Other problems associated with biofilms within water distribution
systems include deterioration of water quality (Le Chevallier & McFeters,
1985) and corrosion of distribution system pipework (Lee et al., 1980;
Walker et al., 1991). The fact that L. pneumophila can derive nutrients
from sources other than the surface supporting its growth explains why
L. pneumophila is frequently isolated from water distribution systems
(Dennis, 1993). The use of polymeric materials to replace traditional
plumbing materials has been on the increase for many years. Organic
compounds which leach from the surfaces of these components provide a
nutrient source for the micro-organisms which colonise them (Ashworth &
Colbourne, 1987a, b). Biofilm formation on such surfaces may lead to a
rapid decrease in water quality leading to a failure to meet the required
standards (Anon., 1982, 1983). L. pneumophila has been found to colonise
rubber sealing washers and gaskets within hot water systems (Dennis,
208                     L. H. G. Morton, S. B. Surman

1993). Rogers et al. (1990) compared a range of different materials used in
plumbing systems for their ability to support the growth of micro-organ-
isms, copper was the most resistant to biofilm formation whilst ethylene-
propylene and latex were the most susceptible. Vess et al. (1993) showed
that the colonisation of PVC pipes by micro-organisms present in the
water can lead to an increased resistance to antimicrobial agents in these
micro-organisms.

Biocorrosion

The mechanisms by which biofilms contribute to corrosion are influenced
by the availability of oxygen in the environment.
   Under aerobic conditions, localised biofilm deposits can cause the
formation of anodic and cathodic areas on the surface of a metal. These
areas become a series of differential chemical cells, each inducing the
transfer of electrons with loss of cations (Videla, 1990). Under aerobic
conditions the utilisation of the hydrocarbons of diesel fuel and aviation
kerosene by Hormoconis resinae, results in the production of organic acids
which are corrosive to metals (Hendey, 1964; Parberry, 1968; Hedrick,
1970). Sulphur oxidising bacteria produce sulphuric acid in quantities
sufficient to bring about the corrosion of metals and concrete (Engvall,
1986). Bacteria and fungi may accelerate corrosion indirectly by utilising
corrosion inhibitors (Prince & Morton, 1988).
   Under anaerobic conditions sulphate reducing bacteria are the major
cause of corrosion in low oxygen or oxygen-free environments. Gaylarde
(1989), lists the various mechanisms by which sulphate reducing bacteria
induce metal disolution. They include:
  (1) cathodic depolarisation brought about by the bacterial enzyme
      hydrogenase,
  (2) the production of corrosive iron sulphides, through the reaction of
      ferrous metals with the hydrogen sulphide released during bacterial
      metabolism,
  (3) sulphide-induced stress corrosion cracking,
  (4) hydrogen-induced cracking or blistering,
  (5) oxidation of biogenic hydrogen sulphide to corrosive elemental
      sulphur; this can occur when oxygen is available in the environ-
      ment.
  The cell walls of Gram-positive bacteria, the outer membranes of
Gram-negative bacteria and their capsules all contain polysaccharides in
various amounts (Gaylarde & Beech, 1989). Polysaccharides in the form
of lipopolysaccharides (LPS) form side chains, which project from Gram-
                           Biofilms in biodeterioration                    209

negative bacterial cell surfaces, and form the interface between other
adjacent cells and/or the surrounding environment (Peterson & Quie,
1981). LPS may selectively bind extracellular cations. This chelating
property has been implicated in the biocorrosion of metals (Beech &
Gaylarde, 1991). The initial conditioning of the surface of a metal by
inorganic and organic molecules is followed by the adhesion of bacterial
cells (Videla, 1990). Extracellular polysaccharide substance (EPS), which
is secreted from some bacterial cells, may enhance the adhesion of these
cells and of those in the immediate vicinity leading to the formation of a
biofilm (Beech & Gaylarde, 1991). EPS has also been implicated in chela-
tion of metal ions (Lieve et al., 1968; Ferris et al., 1987). Attachment of
bacteria such as the sulphate reducer Desulfovibrio vulgaris and the marine
bacterium Vibrio alginolyticus to a metal surface has been shown to result
in rapid metal corrosion (Gaylarde & Johnson, 1980; Gaylarde & Videla,
1987). Hamilton (1985) describes the corrosion of steel drilling platform
legs mediated by sulphate-reducing biofilm micro-organisms releasing
hydrogen sulphide, which attacked the metal. Keevil et al. (1989), in a
survey of a hot water system supplied with soft water, found microbial
biofilm activity associated with copper corrosion. Both aerobic bacteria
and anaerobic sulphate-reducing bacteria (SRB) were implicated, causing
pitting and subsequent perforation of copper pipes.

Plastics

Plastics possess a broad range of chemical and physical properties often
tailored to meet the particular requirements of industry. Specifically they
have been formulated for increased durability and to resist weathering and
therefore to resist microbial biodeterioration. They are both cheap and
relatively easy to produce and consequently they have replaced many
traditional materials such as wood, metal and rubber. Materials which are
commonly considered as plastics include natural and synthetic rubbers,
regenerated and modified celluloses, regenerated proteins, polyethylene,
polypropylene, polystyrene, polyvinyl chloride, polyamides, polyesters
and polyurethanes. Plastics are of great economic importance, with varied
uses such as packaging material and in the manufacture of furniture,
adhesives and inks. The transportation and construction industries are
now using increasing amounts of plastics. There is a wide range of poly-
mer formulations available with differing mechanical and physical prop-
erties. As far as commercial plastics are concerned, it is the plasticisers and
fillers used in the formulations which render them susceptible to attack.
The susceptibility of some plastics is shown in Table 1. This attack usually
manifests itself in the form of a surface biofilm which causes little adverse
210                          L. H. G. Morton, S. B. Surman

                                       TABLE 1
          The Susceptibilityof Some Plastics and Rubber to Microbial Attack
                     Materials                                   A t tacked by
Natural rubber                                         Bacteria and fungi
Synthetic rubbers, e.g.                                Actinomycetes
   butadiene
   polyisoprene
   butyl rubber
Regenerated and modified celluloses                    Bacteria, fungi and actinomycetes
Bulk polymers (commercialplastics), plasticisers and   Bacteria and fungi
fillers in:
   polyethylene
   polyvinylchloride
Polyamides                                             Non-biodegradable
Polyesters -- alkyd resins only                        Fungi and bacteria
Polyurethankes -- polyester polyurethanes only         Fungi and bacteria


effect to the physical or chemical integrity of the material. In some cases,
however, severe cracking can occur, in e.g. in PVC.
   Polyester polyurethanes are particularly susceptible to microbial attack.
These are used in many industrial and commercial applications, for their
strength and their resistance to oxidation, oil and ozone. Their resistance
to impact at decreased temperatures is also a useful property (Ossefort &
Testroet, 1966). However, there is conclusive evidence that polyester
polyurethanes are readily biodegraded by micro-organisms under certain
conditions (Ossefort & Testroet, 1966; Darby & Kaplan, 1968; Rei, 1978;
Inoue, 1982; Seal & Pathirana, 1982; Pathirana & Seal, 1983, 1984a, b;
Wales & Sagar, 1985, 1987; Kay et al., 1993). The term biodegradation
rather than biodeterioration is used here because the material is broken
down to an environmentally acceptable state (Anon., 1983). The degra-
dation processes are thought to be due to hydrolysis cleaving the main
chain ester group and fungal breakdown of the polymer. Kay et al. (1991)
demonstrated the role of bacterial biofilms in the degradation of poly-
urethane foams. They measured changes in the physical integrity of the
material and observed the breakdown of the foam using light microscopy.
Interestingly, the breakdown of the polyurethane was considerably
enhanced by the addition of supplementary nutrients. It has been sugges-
ted (Tokiwa & Suzuki, 1974, 1977; Tokiwa et al., 1976; Fields & Rodri-
guez, 1975; Cook et al., 1981; Pathirana & Seal, 1983, 1984b, 1985a, b;
Wales & Sagar, 1985, 1987; Cameron et al., 1986, 1987; Cameron &
Costas, 1987) that esterase enzyme action is responsible for the microbial
degradation of alkyd resins and polyester polyurethanes. Degradation of
                          Biofilms in biodeterioration                   211

those plasticisers derived from long chain fatty acids has also been shown
to be due to esterolytic action (Berk et al., 1957; Klausmeier, 1966;
Williams et al., 1969; Williams & Dale, 1983). The polyether poly-
urethanes have been shown to be very resistant to attack (Darby &
Kaplan, 1968; Dixit et al., 1971; Pathirana & Seal, 1985a).

Hydrocarbons

Microbial degradation of hydrocarbons occurs in formulations where the
hydrocarbon component is intended to come into contact with water, as is
the case in 'soluble' metal-working fluid emulsions; it also occurs in fuels
and lubricants where water gains access into the fuel or lubricating system,
allowing microbial activity to flourish (Smith, 1990). In such systems there
are effectively four components: water, oil, air and the hydrocarbon-
degrading micro-organisms. Growth in the presence of a water-insoluble
substrate presents problems to such organisms. It is thought that there are
two general types of interaction, pseudosolubilisation which involves the
uptake of fine droplets of oil (less than 1 #m in diameter) from the bulk
phase and that which occurs when there is direct contact between cells and
large oil droplets (Erikson & Nakahara, 1975). Oil-in-water emulsions
may be formed by hydrocarbonoclastic micro-organisms growing on
hydrocarbons (Erikson & Nakahara, 1975; Zajic & Panchal, 1976;
Margaritis et al., 1979; Cooper & Zajic, 1980). Emulsions are formed
either by direct surface action of the micro-organisms or by the produc-
tion of extracellular bioemulsifiers; both actions have the effect of break-
ing down the hydrocarbon to small droplets. This increased mixing of the
oil and water phases increases the accessibility of the hydrocarbon to these
microorganisms. Bioemulsifier-producing micro-organisms will often be
found forming a dense film at the oil-water interface, utilising the emul-
sified hydrocarbon. Prince and Morton (1989) have suggested that in a
two-phase system, a film of micro-organisms developing at the interface
should be regarded as a true biofilm. Biodeterioration of bioemulsifiers
and associated coupling agents caused by microbial contamination in oil
emulsions often results in degradation of the emulsion associated with an
increase in the size of the oil droplets and ultimately the separation of the
two phases (Hill et al., 1976; Hill, 1977). A worrying factor concerning the
bacterial contamination of soluble metal-working fluids is the ability of
pathogens to flourish in such systems (Rossmoore, 1981). The organism
most often implicated in the biodeterioration of hydrocarbon fuels is
Hormoconis resinae (Lindau) de Vries, syn. Cladosporium resinae (Lindau)
de Vreis, the imperfect form of Amorphotheca resinae, Parberry. The
biodeterioration of fuel oils in turbine engines, including marine engines
212                      L. H. G. Morton, S. B. Surman

and also jet fuels has been ascribed to H. resinae (Parberry, 1971; Park,
1975; Houghton & Gage, 1979; Smith & Crook, 1980; May & Niehof,
1981). Water which remains in the small crevices and seams in fuel tanks
provides an ideal environment for H. resinae to colonis e, spreading over
the oil-water interface, providing ideal conditions for further water
catchment (Elphick & Hunter, 1968). The removal of H. resinae from the
tanks is not an easy task, the mycelia being firmly attached to the surfaces.
Fuel oils may be subject to biodeterioration by H. resinae (Cofone et al.,
1973; Teh & Lee, 1974). This ability to metabolise such a range of hydro-
carbons (Cooney & Proby, 1971; Walker & Cooney, 1973), can result in
the development of thick mycelial mats formed by the growth of H. resi-
nae at the oil-water interface. The acid produced may lead to an increase
in the rate of corrosion of the fuel tanks due to the decrease in pH.
However, because of the rapid rate at which the fuel is used and the large
volumes that the tanks hold, little discernible deterioration of the fuel
itself is observed (Hill, 1978). The main problem resulting from this
contamination is the blockage of fuel lines and filters and the shorting of
the capacitive probes of fuel gauges (Williams & Lugg, 1980). More
recently it has been observed that the synthetic metal working fluids may
become contaminated by fungi. Fungal biofilms resulting in free floating
biomass often cause real problems in industry today. Prince and Morton
(1988) have shown that certain susceptible components of a formulation
are readily attacked by fungi including pathogenic forms.

Biofilms on the surfaces of buildings and monuments

Two main groups of microorganisms, algae and fungi are known to colo-
nise the external surfaces of buildings and monuments giving the surface a
dirty, neglected and unsightly appearance (Perrichet, 1987). In addition,
they are considered to be the forerunners of lichens, mosses and higher
plants capable of extensive corrosive activity. In terrestrial environments,
epiphytic algal growths will occur on surfaces where conditions of damp-
ness, warmth and light are conducive for their growth (Hueck-van der
Plas, 1968; Whitely, 1973; Richardson, 1973; Springle, 1979; Morton,
1979). The chelation of cations by microbially produced organic acids is
believed to play an important role in the deterioration of stone building
materials (Wainwright et al., 1993). Whilst algal growths are not believed
to play a significant role in the assimilative biodeterioration of the
formulation components of external coatings, they may have profound
effects on the soundness of a building. The majority of algal genera
involved belong to the Chlorophyceae and Cyanophyceae with species of
Pleuro¢occus, Stichococcus, Trentepohlia, Oscillatoria and S c y t o n e m a
                           Biofilms in biodeterioration                   213

being particularly implicated (Gillatt & Tracey, 1987). Apart from the
obvious undesirable effects on the appearance of the surface, major
problems may occur due to algal water retention during winter months.
Repeated freezing and thawing of the hydrated algae contribute further to
the deterioration of a surface and this may be a contributory factor to
causing damp in such a building.

Biofilms on painted surfaces and surface coating

On internal coatings, however, fungi have been recognised as being the
main deteriorgens. The genera most often incriminated include
Aureobasidium, Cladosporium, Aspergillus and Penicillium (Gillatt &
Tracey, 1987). The initial disfigurement of interior decorative surfaces by
these organisms may have far-reaching consequences, because as they are
able to metabolise some of the components of the interior coating formu-
lations they may expose underlying structural materials, such as timber
and metal, leaving these open to attack by a range of micro-organisms
(Morton, 1987), these may include pathogenic, or more correctly aller-
genic fungi. The health-related aspects of such fungal colonisation in
damp, ill-ventilated dwellings is becoming an increasing cause for concern.
Oligotrophic fungi may also grow on painted surfaces obtaining nutrients
not from the surface itself but from airborne dust and organic substances,
this occurs particularly in areas of high humidity.


                              CONCLUSION

Biofilms form when adherent micro-organisms colonise surfaces. Bacterial
adhesion is by means of a glycocalyx, a hydrated polyanionic poly-
saccharide matrix, which can act as an ionic exchange matrix. In the
aqueous environment nutrients are concentrated in the biofilm and
subsequent metabolic activity intensifies with resulting substrate depletion
or damage. A biofilm can be an effective barrier against antimicrobial
agents.


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