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					                                      International Biodeterioration & Biodegradation 53 (2004) 177 – 183
                                                                                                                  www.elsevier.com/locate/ibiod




       Corrosion of technical materials in the presence of bioÿlms—current
               understanding and state-of-the art methods of study
                                                              Iwona B. Beech∗
  School of Pharmacy and Biomedical Sciences,University of Portsmouth, St. Michael’s Building White Swan Road, Portsmouth P01 2DT, UK




Abstract

   It is documented that bioÿlms are capable of in uencing electrochemical processes at the metal surface, often leading to deterioration
of metals referred to as biocorrosion or microbiologically in uenced corrosion. Bioÿlms typically consist of microbial cells and their
metabolic products including extracellular polymers, and inorganic precipitates. Interaction of bioÿlms and exopolymers with metal ions
has long been proposed as one of the mechanisms of metal biodeterioration.
   This paper presents an overview of the application of modern microscopy and surface analysis techniques in studying the involvement
of bioÿlms and extracellular polymeric material in the biocorrosion process of metals and their alloys.
? 2003 Elsevier Ltd. All rights reserved.




1. Bioÿlms and biodeterioration                                                between microbial cells, or products of their metabolism
                                                                               such as EPS, and the surface is established (Gaylarde and
   The term bioÿlm refers to the development of microbial                      Johnston, 1982; Gaylarde and Videla, 1987).
communities on submerged surfaces in aqueous environ-
ments (Characklis and Marshall, 1990). The growth of
bioÿlm is considered to be a result of complex processes                       2. Interaction of bacterial exopolymers with metals
involving transport of organic and inorganic molecules and
microbial cells to the surface, adsorption of molecules to                        It is unequivocally accepted that microbial exopolymers,
the surface (formation of the conditioning layer) and initial                  including lipopolysaccharides (LPS), play an important
attachment of microbial cells followed by their irreversible                   role in the process of cell attachment to metal surfaces
adhesion facilitated by production of extracellular poly-                      (Beech and Gaylarde, 1989; Flemming et al., 1998). The
meric substances (EPS), often referred to as the glycocalyx                    EPS consist of lipids, polysaccharides, proteins and nucleic
or slime (Costerton et al., 1978). The biofouling and biode-                   acids (Wingender et al., 1999). The content of these macro-
terioration of man-made materials, including metal and their                   molecules in EPS varies, depending on bacterial species
alloys, due to the bioÿlm formation has great environmental                    and growth conditions (Sutherland, 1985; Beech et al.,
and economical implications. Many industrial sectors such                      1991a; Beech et al., 1999a). Although in planktonic bacte-
as gas, oil, nuclear power, shipping, aircraft, chemical and                   ria, EPS are often present as a capsule, exopolymers do not
civil engineering su er potential pollution problems, health                   have to be associated with cells but can also be released
and safety hazards and substantial ÿnancial losses as a result                 into the bulk phase of surrounding liquid. The “free” EPS
of bioÿlm development (Hamilton, 1985; Flemming, 1996).                        material can compete with bacterial cells for binding sites
Several models are proposed to explain possible mechanisms                     at the metal surface and thus needs to be considered when
by which bioÿlms can in uence deterioration of metals                          investigating biocorrosion (Paradies et al., 1992).
(Borenstein, 1994). It has been documented that degrada-                          One of the important properties of EPS is their ability to
tion of metal surfaces, also termed biocorrosion or micro-                     complex with metal ions (Geesey and Mittelman, 1985).
bially in uenced corrosion (MIC), occurs when the contact                      Most of the available information on the EPS-mediated
                                                                               mechanism of metal accumulation has been generated in
  ∗   Tel.: +44-1705-842147; fax: +44-1705-842147.                             waste treatment research. Many purpose-built systems for
      E-mail address: iwona.beech@port.ac.uk (I.B. Beech).                     metal removal from wastewaters use immobilized living

0964-8305/$ - see front matter ? 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0964-8305(03)00092-1
178                           I.B. Beech / International Biodeterioration & Biodegradation 53 (2004) 177 – 183


microorganisms. In some of these systems, bacterial cells                conditions, carrying a charge that promotes ionic and elec-
colonize support materials such as glass, stainless steel                trostatic binding of counterions, including metals. Several
wire, wood shavings, reticulated foams and polyvinyl chlo-               classes of polymeric molecules participate in EPS/metal in-
ride to form bioÿlms. Such bioÿlms have been shown to be                 teractions by formation of salt bridges with carboxyl groups
very e cient in immobilizing metal ion species (Macaskie                 on acidic polymers, i.e. polysaccharides containing uronic
and Dean, 1987). Although the role of exopolymers present                acids, and by forming weak electrostatic bonds with hy-
within these bioÿlms in the removal of metal ion species has             droxyl groups on polymers containing neutral carbohydrates.
not been considered, it is likely that EPS could contribute              A large number of metals have been reported to cross-link
to this process.                                                         polysaccharides (Geesey and Jang, 1989).
   As already stated, one of the functions of EPS is to en-                 In acid mine drainage waters heterotrophic bacteria, often
hance the ability of cells to adhere to surfaces (Fletcher               referred to as “acid streamers”, produce copious amounts of
and Floodgate, 1973; Marshall, 1992). Nutrients, which are               slime consisting of a ÿbrillar polymer network. This extra-
scarce in aquatic environments, are concentrated on surfaces             cellular material has been reported to be a mixture of neutral
(Characklis and Marshall, 1990). The colonization of the                 and acidic polysaccharides and RNA (Johnson and Kelso,
surface would therefore prove to be highly advantageous                  1981). Further studies by Johnson et al. (1993) showed that
for cells capable of attaching to it. Studies on EPS produc-             the acid streamers participated in oxido-reduction of iron,
tion by Pseudomonas atlantica showed the expression of                   and that iron was bound within the exopolymer matrix of the
EPS to be variable and controlled by genome rearrangement                streamers. It can be speculated that carboxylic groups orig-
(Bartlett et al., 1988). The authors speculated that recombi-            inating from the carbohydrate component of the EPS and
nal switches to generate diversity in a population exist, with           phosphate groups liberated during nucleic acid degradation
the result that a small fraction of the population could take            could play a part in the binding of metals, e.g. iron, increas-
advantage of favourable circumstances. The presence of a                 ing the overall metal binding capacity of EPS. The latter
nutrient rich surface could provide that trigger. Thus, cells            property of bacterial EPS contributes to the formation of
would regulate the secretion of EPS in response to the pres-             metal concentration cells and promotes galvanic coupling,
ence of the surface (Beech et al., 1991b). Evidence has been             thus in uencing the electrochemical behavior of metal (Ford
presented to support this theory by the revelation that expres-          et al., 1987; White et al., 1985). Indeed, evidence exists that
sion of certain genes can be modiÿed following association               exopolymers exhibit great selectivity in complexing metal
of bacteria with a surface (Davies et al., 1994). Examination            ions, and a direct involvement of EPS in the biodeteriora-
of protein proÿles in EPS of marine sulphate-reducing bac-               tion of metal surfaces such as stainless steel, copper and car-
teria (SRB) isolates, revealed the appearance of new bands               bon steel has been shown (Angell et al., 1995; Thies et al.,
in exopolymers harvested from cultures grown in the pres-                1995; Beech et al., 1996). There is, however, a controversy
ence of mild steel surfaces, thus further conÿrming the e ect            regarding the type of EPS fraction playing a key role in in-
of surface on cell metabolism (Zinkevich et al., 1996).                  teractions with metals. Some reports indicate that proteins
   It can be proposed that interaction between bacterial sur-            are involved (Angell and Chamberlain, 1991), while others
face molecules such as LPS and/or EPS and metal ions                     emphasize the role of the polysaccharide component of EPS
released at the metal/liquid interface can be regulated by               in metal/bacteria interaction (Geesey and Jang, 1990). De-
the abundance of metal ion species (Gaylarde and Beech,                  spite all the research e ort focusing on the involvement of
1988). All bacteria require metal ions for their growth. The             exopolymers in metal deterioration, very little (if any) infor-
availability and the type of ions (type of metal species and             mation is available on the synthesis and chemical structure
their reactivity determined by the metal oxidation state) are            of bacterial EPS within bioÿlms formed on metal surfaces
likely to have an e ect on the colonization of a metal surface           and the types of EPS macromolecule that are involved in
(Beech et al., 1993). The chemistry of the surface could af-             interacting with metal ions at the surface. E orts are there-
fect bacterial population positively or adversely, in the ÿrst           fore made to apply surface analysis techniques to gain a new
case by facilitating the attachment of cells to the surface via          insight into these phenomena (Gubner and Beech, 2000;
binding of metal ions by EPS and/or LPS (Beech, 1990 and                 Beech et al., 2000a).
references therein), and in the second case by preventing
surface colonization due to the toxic e ect of some of the
metal ion species, e.g. Cr (Percival et al., 1997). The former           3. The use of microscopy and surface science to study
phenomenon would favour attachment and development of                    bioÿlm/metal interactions
a bioÿlm, often leading to severe fouling and deterioration
of metal. The latter case would result in the partial inhibition            The forms of deterioration which can be stimulated by
of bacterial adhesion and decrease in fouling, consequently              the interaction of bioÿlms with metals are numerous and a
limiting the degree of material damage.                                  variety of techniques are employed to link biodeterioration
   The interactions between bacterial EPS and metal ions                 to microbial activities at surfaces (Beech, 1999; Beech and
are documented (Ford et al., 1988). Many exopolymers                     Coutinho, 2003). Chemical spectroscopy at surfaces o ers
of aquatic microorganisms act as polyanions under natural                qualitative and semi-quantitative information on the nature
                              I.B. Beech / International Biodeterioration & Biodegradation 53 (2004) 177 – 183                    179


of the deterioration products that have accumulated on a                 relevant analytical signal is measured at each position in
metal surface. Spatially resolved surface chemistry obtained             the scanned area to generate an image of the sample. PIXE
with spectroscopic instrumentation should then be related to             analysis measures X-rays produced from the sample. Unlike
spatially resolved microbiology at the same location, a pro-             EDX, PIXE uses MeV protons rather than keV electrons,
cedure that requires image registration and alignment. The               thus generating less secondary radiation. This makes PIXE
latter has only recently been applied to processes involv-               a more sensitive technique than EDX for imaging trace ele-
ing interaction of bioÿlms with metals (Geesey et al., 1996;             ment distribution. Applications of PIXE in biology are nu-
Pendyala et al., 1996; Suci et al., 1997; Beech et al., 1999b).          merous, ranging from studies of calcium and barium uptake
                                                                         in green algae, or investigation of elemental variation and
                                                                         metal accumulation in a germinating fungus, to elemental
3.1. Microscopy
                                                                         analysis of diseased human tissue (Breese et al., 1992.). Be-
                                                                         cause of its resolving power and sensitivity, this technique
   The contributions of bioÿlms to metal deterioration
                                                                         is currently being applied to the study of metal distribution
is usually qualitatively assessed using scanning electron
                                                                         within the bioÿlms developed by marine Pseudomonas sp.
microscopy (SEM), environmental scanning electron mi-
                                                                         on stainless steel surfaces (Beech, unpublished).
croscopy (ESEM) and atomic force microscopy (AFM).
                                                                            Auger electron spectroscopy (AES) has been used to
Re ected di erential interference contrast microscopy
                                                                         investigate biocorrosion of condenser tubes (Chen et al.,
(DIC) can also be employed where the metal surface pro-
                                                                         1988). The technique gives elemental abundance only in the
vides su cient re ective properties to resolve attached
                                                                         top few nanometers of the surface at very high spatial reso-
microorganisms (Surman et al., 1996). Recently, confocal
                                                                         lution. This allows mapping of corrosion products across a
scanning laser microscopy (CSLM) has also been used to
                                                                         metal surface that has experienced localized attack. Surface
provide three-dimensional information on the bioÿlm/metal
                                                                         contamination by organics and other material can interfere
surface interaction (Walker et al., 1998).
                                                                         with detection of the underlying corrosion products when
   Microscopy provides information about the morphology
                                                                         using such a surface-sensitive technique.
of microbial cells and colonies, the distribution of micro-
                                                                            Mossbauer spectroscopy can be applied to detect
bial colonies on the surface, presence of EPS and the nature
                                                                         iron-containing compounds. It has been employed to detect
of corrosion products (crystalline or amorphous). It also re-
                                                                         “green rust 2” among corrosion products of steel exposed
veals the type of attack by revealing changes in metal mi-
                                                                         to marine sediments containing SRB (Olowe et al., 1991,
crostructure after removal of the bioÿlm (Little et al., 1991;
                                                                         1992). Since samples for XRD, EDS, AES and XPS ana-
Wagner and Ray, 1994; Beech et al., 1996 and references
                                                                         lysis must be dehydrated as they are analysed in vacuo,
therein). Recent review on the use of microscopy techniques
                                                                         some distortion and reorientation of surface-associated ma-
for the study of bioÿlms is provided by Beech et al. (2000b,
                                                                         terial can be anticipated. Care must also be taken to avoid
2002).
                                                                         changes in the oxidation state of some corrosion products
                                                                         during dehydration.
3.2. Surface analysis                                                       Attenuated total re ectance Fourier transform infrared
                                                                         spectroscopy (ATR/FT-IR) has been applied to quantify
   Surface chemical analysis allows determination of the                 the rate of dissolution of a thin metal ÿlm deposited on an
chemical composition of corrosion products and micro-                    internal re ectance element exposed to either owing or
biological deposits, and thus the opportunity to gain                    stagnant aqueous media containing microorganisms and
insight into the electrochemical reactions involved in                   products of their metabolism. The method is based on the
the bioÿlm-in uenced metal deterioration process. X-ray                  observation that water absorbance in the infrared region
di raction (XRD) and energy dispersive X-ray analysis                    increases as the thickness of the thin ÿlm decreases due to
(EDS or EDX) have been widely used to obtain elemen-                     metal deterioration. Changes in the thickness of the metal
tal information on corrosion products on metal surfaces                  ÿlm corresponding to a few atomic layers can be detected
(Marquis, 1989). XRD has limited application to biocor-                  and the measurements are obtained non-destructively in
rosion, as it does not possess the high spatial resolution               real time. This approach has been used to demonstrate the
to detect localized attack. EDX assesses elemental abun-                 participation of a microbial bioÿlm in the localized attack
dance at high spatial resolution over a sampling depth of                on copper ÿlm (Bremer and Geesey, 1991); it revealed cor-
approximately 1 m. Depending on the thickness of the                     relation between the onset of corrosion and the synthesis of
corrosion deposit, EDX may provide elemental information                 EPS during bioÿlm formation on the ÿlm. ATR/FT-IR has
on not only corrosion products but also the underlying bulk              also been employed to demonstrate that the exopolysaccha-
material.                                                                ride produced by the marine bacterium Pseudoalteromonas
   Particle-induced X-ray emission spectroscopy (PIXE)                   (Pseudomonas) atlantica has an in uence on the corrosion
is a form of nuclear microprobe (NM). In the NM a fo-                    of copper (Jolley et al., 1989).
cused beam of MeV light ions (most commonly protons) is                     Most of the investigations of metal binding by either
scanned across the sample surface, and the strength of the               microbial biomass or EPS material employ techniques of
180                          I.B. Beech / International Biodeterioration & Biodegradation 53 (2004) 177 – 183


analytical chemistry such as atomic absorption spectro-                 of metals has, so far, been limited to studies involving
metry, polarography and inductively coupled plasma                      biocorrosion of copper (Geesey et al., 2000) and stainless
spectrometry (ICP). Such methods often require a sub-                   steel (Pendyala et al., 1996; Beech et al., 1998b, 1999a).
stantial quantity of sample (mg) in order to detect                     The technique has been employed to study the ef-
parts-per-billion (ppb) levels of metals, thus demand-                  fect of bacterial bioÿlms and exopolymers on the
ing large-scale puriÿcation of samples, which is often                  composition of passive layers formed on AISI 304 and
expensive and not always feasible. In contrast, mod-                    316 stainless steel. The thickness of the passive layers, the
ern techniques of surface science such as time-of- ight                 distribution of the alloying elements within the layers, and
secondary ionization mass spectrometry (TOF-SIMS)                       the level of layer hydration, changed signiÿcantly when the
and X-ray photoelectron spectroscopy (XPS) are well                     bioÿlm was present, compromising corrosion resistance of
suited to study interaction of metals with biological                   steel.
material using a small (ng) sample size (Muddlman
et al., 1994; Baty et al., 1996; Beech et al., 1998a).
                                                                        3.2.2. Time-of- ight secondary ionization mass
                                                                        spectrometry
3.2.1. X-ray photoelectron spectroscopy                                    TOF-SIMS is a high vacuum (HV) technique employ-
   XPS or electron spectroscopy for chemical analysis                   ing a pulsed ion beam of, e.g., Cs or Ga (primary ions) to
(ESCA) provides direct chemical characterization of the                 sputter the outermost surface of the sample (approximately
samples’ surface layer (2–5 nm depth). XPS involves ex-                 1 nm depth). The majority of the sputtered material is in the
posure of the sample to an X-ray beam in order to emit                  form of neutral atoms and molecules, but a certain percent-
electrons. The kinetic energy of the emitted core electrons             age of this material is emitted as either positively or nega-
(photoelectrons) is analysed, and their binding energy, EB ,            tively charged ions. These “secondary ions” generated by a
determined according to the photoelectric e ect EB =h −Ee ,             primary ion pulse on the target surface are electrostatically
where h is the energy of the incident radiation (X-rays) and            collected, accelerated into a “ ight tube”, and their mass
Ee is the measured kinetic energy of the photoelectron. The             determined by monitoring the time at which the ions reach
spectrum is obtained as a plot of the number of electrons               the mass detector. The exact masses are known with such
per energy interval vs. their binding energy. The changes in            accuracy that particles with the same nominal mass can be
the core level EB , or chemical shifts, are due to alterations          distinguished from one another. Mass resolution of 0.000X
in the electron density of the valence shell. A more highly             (four decimal points) atomic mass units (amu) and a mass
oxidized species gives rise to a higher EB , while a more               range from 0 to 10 000 amu can be obtained. The data is
reduced species shows the opposite e ect. Each peak of                  displayed in a secondary ion signal intensity vs. amu format.
the recorded spectrum is characteristic of a given energy               The spectra produce unique patterns that vary according to
level of an element which is in uenced by the chemical                  the structure of the material.
state of the element, mainly the electron density resulting                Although SIMS o ers greater chemical selectivity and
from chemical bonds made with neighbouring atoms. Most                  surface sensitivity than XPS and has been widely used to
elements have major photoelectron peaks below 1100 eV,                  study organic compounds (Siegbahn et al., 1967; Hercules,
and so a scan range from 1100 –0 eV binding energy is                   1993), it has only recently been considered in applications
usually su cient to identify all detectable elements (a sur-            such as characterization of microbial cells and bioadhesives.
vey scan). For the purpose of chemical state identiÿcation,             Techniques of XPS and TOF-SIMS helped to evaluate bind-
for quantitative analysis of minor components and for peak              ing of Fe ions originating from mild steel by exopolymers
deconvolution, detailed scans are obtained (high-resolution             recovered from cultures of two marine SRB species (Ind1
scans or multiplex scans). Quantitative data is obtained                and Al1 strains) of the genus Desulfovibrio. Previous work
from peak heights or peak areas, and identiÿcation of                   demonstrated that under identical growth conditions the
chemical states is made from exact measurements of peak                 two SRB strains, although having similar growth rates and
positions and separations, as well as from certain spectral             sulphate-reduction rates, di ered in their aggressiveness to-
features such as the shape of the peaks.                                wards mild steel (Videla et al., 1996). Bioÿlms formed by
   XPS has been applied to investigations of micro-                     strain Ind1 caused greater deterioration of steel than those of
organisms, proteins and microbial adhesins on non-metallic              strain Al1 (Cheung, 1995). One of the marked di erences
surfaces (Rouxhet et al., 1994 and references therein; Sosa             between the Ind1 and Al1 was the yield and composition of
et al., 1994). However, the technique has limited ability to            their EPS (Zinkevich et al., 1996). Furthermore, the exo-
provide detailed molecular information, particularly when               polymer of Ind1 was corrosive towards mild steel, causing
atoms are in a wide variety of chemical states, as is the               increased Fe dissolution, which resulted in extensive pitting
case for macromolecules such as carbohydrates and pro-                  of steel (Beech et al., 1998c). The application of TOF-SIMS
teins. XPS is often employed to study bonding in metal                  and XPS helped to reveal the di erences in Fe binding by
compounds (Carver et al., 1972 and references therein);                 the EPS produced by both strains, demonstrating that of the
however, its application in the ÿeld of biodeterioration                two, Ind1 EPS had much higher a nity for Fe uptake. In
                                  I.B. Beech / International Biodeterioration & Biodegradation 53 (2004) 177 – 183                                   181


addition, XPS spectra strongly indicated that in each type                      Characteristics, Analysis and Control. Institute of Water Analysis
of EPS, Fe was present in a di erent chemical environment                       Publishing of Alliance House, Ch. 8.
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                                                                                desulfuricans and Pseudomonas uorescens to mild steel surfaces.
of macromolecule were participating in the Fe binding pro-                      Journal of Applied Bacteriology 67, 201–207.
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as Fe2+ was associated with EPS as Fe3+ ion (Beech et al.,                      Polysaccharides in bioÿlms and in free EPS of D. desulfuricans in
1999c).                                                                         the presence of mild and stainless steel and their role in corrosion.
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to environmental conditions conducive for the formation of                      Microbiology and Biotechnology 35, 65–71.
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damage, occurs as a result of the activity of physiologi-                       chemistry in SRB in uenced corrosion of steel. International Journal
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                                                                                Comparative studies of bacterial bioÿlms on steel surfaces using
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ized chemical gradients at the metal surface. The presence of                   microscopy. Biofouling 10, 65–77.
such chemical gradients facilitates the development of elec-                 Beech, I.B., Zinkevich, V., Tapper, R., Avci, R., 1998a. The interaction of
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                                                                             Beech, I.B., Zinkevich, V., Hanjangsit, L., Smith, J., Gubner, R., Avci,
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