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: email@example.com (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. within the organic matrix. This implied that di erent types Beech, I.B., Gaylarde, C.C., 1989. Adhesion of Desulfovibrio desulfuricans and Pseudomonas uorescens to mild steel surfaces. of macromolecule were participating in the Fe binding pro- Journal of Applied Bacteriology 67, 201–207. cess. Furthermore, iron released from the surface of steel Beech, I.B., Gaylarde, C.C., Smith, J.J., Geesey, G.G., 1991a. 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. In: Dowling, N.J., Mittelman, M.W., Danko, J.C. (Eds.), Microbially In uenced Corrosion and Biodeterioration. University of Tennessee 4. Summary Occasional Publication, Knoxville, Tennessee, USA, pp. 2/53–2/58. 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