Environ. Sci. Technol. 2008, 42, 2233–2242
Enzymatic Approach in Microbial-Influenced Corrosion: A Review Based on Stainless Steels in Natural Waters J . L A N D O U L S I , * ,† K . E L K I R A T , § C . R I C H A R D , † D. FÉRON,4 AND S. PULVIN‡ Laboratoire Roberval, CNRS UMR 6253, Génie enzymatique et cellulaire, CNRS UMR 6022, and Laboratoire de Biomécanique et Bioingénierie, CNRS UMR 6600, Université de Technologie de Compiègne (UTC), BP 20529, F-60205 Compiègne Cedex, France, and CEA/DEN-Saclay, Service de la corrosion et du comportement des matériaux dans leur environnement, Bât. 458 PC50, 91191 Gif-sur-Yvette Cedex, France
Received July 24, 2007. Revised manuscript received December 18, 2007. Accepted January 4, 2008.
The electrochemical behavior of stainless steels (SS) in natural waters is characterized by the ennoblement of their free corrosion potential (Ecorr). This phenomenon depends strongly on the settlement of biofilms on SS surfaces. Many hypotheses have been proposed to explain the biofilm action, in particular the enzymatic catalysis plays an important role by shifting the cathodic and/or anodic processes. However, there are still only few studies relating the use of purified enzymes. In contrast with bacteria-associated corrosion, the direct influence of enzymes is still poorly documented. The aim of this review is to show the benefits of the enzymatic approach in the study of biocorrosion. Indeed, enzymatic systems may constitute convenient models to mimic microbial influenced corrosion and to evaluate the behavior of metallic materials in natural waters.
1. Introduction Corrosion is an interfacial process leading to surface degradation. It involves electrochemical reactions between the material and its environment. In aqueous media, these reactions are governed by physicochemical parameters (pH, redox potential, conductivity, etc). Microorganisms may also influence deeply this process: they may initiate or accelerate the surface degradation and they do so in the form of biofilms (1). This microbial layer forms as a result of the adhesion and growth of microorganisms on surfaces. It corresponds to the formation of a complex hydrated matrix including polysaccharides and proteins (1). Cell metabolites accumulate and enhance corrosion by changing the local physicochemical conditions. This phenomenon is commonly called “microbial influenced or induced corrosion” (MIC). Many metallic materials may be submitted to MIC in natural waters (seawater, rivers, lakes, etc) in which the bacterial population is estimated to be between 103 and 107 cells/mL (2). Numerous authors investigated the role of microbial extracellular molecules, including enzymes, and * Corresponding author. E-mail:
[email protected]. Tel: +33 344 237 334. Fax: +33 344 234 689. † Laboratoire Roberval, CNRS UMR 6253 (UTC). § Laboratoire de Biomécanique et Bioingénierie, CNRS UMR 6600 (UTC). 4 Service de la corrosion et du comportement des matériaux dans leur environnement (CEA/DEN). ‡ Génie Enzymatique et Cellulaire, CNRS UMR 6022 (UTC). 10.1021/es071830g CCC: $40.75
Published on Web 02/28/2008
2008 American Chemical Society
found out that they are able to affect the electrochemical behavior of stainless steels (SS) (3–7). However, corrosion studies using purified enzymes to study MIC are still poorly reported in the literature, probably because of the following main reasons: 1. Since proteins are very sensitive to environmental conditions, their catalytic activity may change dramatically, or they may be denatured, due to the corrosion test conditions. 2. Even if some bacteria provoking corrosion are already well-known, the enzymes which may have a key role in the MIC processes are still not fully identified. This lack of information may be due to the complexity of microorganism’s metabolic activities. The aim of this review is to point out the importance of the enzymatic approach in the study of MIC. The analysis of the different hypothesis reported in the literature evidence a promising connection between enzymatic reactions and the electrochemical response.
2. Behavior of SS in Natural Waters 2.1. Potential Ennoblement. The corrosion of SS has attracted much interest because of their wide use in natural waters. Their behavior is strongly affected by the presence of biofilms on their surface (8, 9). The open circuit potential (OCP), or free corrosion potential (Ecorr), is the first indicator used to characterize the influence of biofilms on the electrochemical behavior of SS. During a 30-day immersion period in seawater, potential ennoblement progressed until the Ecorr reached high values: +300 to +400 mV/SCE (3, 8–10). However, in sterile seawater, Ecorr never exceeds +100 mV/ SCE (3, 8, 9, 11). In European programs (12–14), numerous electrochemical tests have been performed in different seawaters and showed that ennoblement occurs in all cases (Figure 1). Ennoblement on SS was also observed after immersion in waters with low chloride concentration such as rivers, lakes and estuaries: Ecorr reached values between + 200 and + 400 mV/SCE (Figure 2) (15–19). In all cases, the chemical composition and the microstructure of SS have no influence on the tendency of the metal to ennoble as long as it is able to form a passive layer (8, 20–22). These parameters rather influence the time which precedes ennoblement called “incubation time” and the rate of potential increase, mainly affected by biological (biofilm VOL. 42, NO. 7, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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passive layer, by using electrochemical impedance spectroscopy. A corrosion mechanism based on the cathodic depolarization was proposed. The authors assumed that SRB contains a hydrogenase activity (molecular hydrogenactivating enzyme) which removes hydrogen from the surface of Fe in order to reduce sulfate (see section 3.2 for details).
3. The Involvement of Enzymes in MIC FIGURE 1. Average Ecorr versus time measured along summertime tests in European Seas on stainless steel plates (13).
FIGURE 2. Ecorr vs time for three 316 L stainless steel coupons during in situ exposure to the Seine River (19). nature, morphology, etc) and physicochemical factors (temperature, hydrodynamic factors). 1.2. Anodic and Cathodic Shifts. The corrosion rate is imposed by the slowest partial reaction, either anodic or cathodic. The evolution of the biofilm/metal interface may provoke a shift in the anodic or the cathodic process. In most of the previous studies, the ennoblement was found to be associated with an increase of the cathodic current density (23–26). The influence of biofilms on the passive current density is contradictory. In some cases, no effect attributable to biofilm was observed (3, 27). Salvago et al. (28, 29) performed tests in seawater using three austenitic SS and their results showed that biofilm affects both cathodic and anodic polarization branches. In these experiments, the ennoblement of Ecorr was ranging from -200 mV/SCE to +400 mV/SCE. Figure 3 is a schematic representation which explains how Ecorr ennoblement can be induced by either the cathodic or the anodic shifts. 2.3. Evolution of SS Passive Film Properties. SS are autopassivable alloys: they form a thin oxide layer, typically with a thickness of a few nanometers (30). Changes in potential or anion concentration in the electrolyte forces the passive film to adapt. Therefore, the time required to respond to environmental changes is a very important factor for the stability of the passive film. The problem with MIC is to understand once the biofilm has been formed, how metabolic activities of cells induce modifications to the passive layer and how such modifications result in changes to the rates of the anodic and/or cathodic processes as depicted in Figure 3. Many authors have observed that the modifications in the properties of the SS oxide layer in natural waters depend strongly on the bacterial population (31–37). Geesey et al. (33) observed a selective colonization of the SS surface by Citrobacter freundii (facultative anaerobic bacteria) resulting in a significant depletion of Cr relative to Ni. By contrast, when C. freundii was in coculture with Desulfovibrio gigas, a depletion of Fe relative to Ni was evidenced (33). Recently, a similar depletion of Fe and an enrichment of Cr were observed on SS in the presence of Pseudomonas NCIMB 2021 bacteria (37). Gonzalez et al. (32) observed that sulfate-reducing bacteria (SRB), affect strongly the electrochemical properties of the 2234
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3.1. Mechanisms in Aerobic MIC. The description of biofilms has evolved from the uniform representation of Hamilton et al. (38) to the mushroom-shaped model described by Costerton et al. (39). It is extremely difficult to generalize about biofilm structure and physiological activities (39). However, it is commonly assumed that the particular structure of biofilms allows the flow of nutrients, enzymes, metabolites, waste products, and other solutes (39–42). In fact, according to Sutherland (41), the biofilm matrix may be considered as a system of immobilized enzymes in which the medium and the enzyme activities are constantly changing and evolving to reach an approximately steady state. 3.1.1. Oxygen Reduction: Abiotic vs Biotic Mechanisms. Under MIC conditions, the colonization and growth of bacteria on the metal surface give rise to a biofilm which displays a nonuniform coverage on the surface (43). Mattila et al. (44) have used microscopic techniques to observe the SS surface after immersion in seawater: it was only partially covered with a biofilm. These observations suggest that oxygen may have some free access to the metal surface in agreement with a previous study (40). Therefore, the biofilm physically hinders only a part of oxygen diffusion toward the metallic surface. The oxygen concentration profile inside the biofilm is difficult to determine with accuracy because of the heterogeneity of biofilms. With the help of a microelectrode technique, Xu et al. (45) have observed that oxygen concentration decreases with increasing depth into the biofilm. Recently, a three-dimensional mapping of oxygen distribution in wastewater biofilms was obtained (46). It revealed the existence of some highly concentrated pockets of oxygen within the biofilm (46). Lewandowski et al. (47) have proposed a bactericide treatment with glutaraldehyde to eliminate oxygen consumption by microorganisms in biofilm formed in seawater. Their experiments showed how the oxygen consumption through metabolic pathways in the biofilm influences its availability at the metal/biofilm interface. Consequently, oxygen gradients result from its diffusion in the biofilm and from its consumption in metabolic pathways as well. In microorganisms, oxygen acts as a final electron acceptor. The major part of oxygen undergoes a four-electron-pathway reduction in microorganisms, according to the reaction (1). This reaction is catalyzed by cytochrome-c oxidase (EC 1.9.3.1). [The EC number (Enzyme Commission number) is a numerical classification scheme for enzymes, based on the chemical reactions they catalyze. As a system of enzyme nomenclature, every EC number is associated with a recommended name for the respective enzyme (48)]. +
O2 + 4e- f 4H + 2H2O
(1)
However, to minimize the energy gap, the reaction (1) is generally a succession of many electron reactions. In this case, oxygen may be subjected to one-electron biological reductions. This may lead to the formation of radical or molecular intermediate products, called reactive oxygen species (ROS) because of their higher reactivity than the oxygen itself. The four steps of one-electron biological oxygen reduction and ROS are presented in Figure 4. Under abiotic conditions, the oxygen reduction on metallic substrates is thermodynamically possible. Although
FIGURE 3. Hypothetical polarization curves of the cathodic and anodic processes on stainless steel under MIC conditions: cathodic (a) or anodic (b) shift. In panel a, the cathodic reaction rate increased while the passive anodic curve is unchanged. Another possibility is illustrated in panel b, the cathodic curve is unchanged while the passive anodic current decreases. In both cases, these mechanisms result in the shift of Ecorr towards anodic values.
FIGURE 4. Intermediates species of one-electron oxygen reduction: reactive oxygen species. the rate of this reaction is very slow, it may be catalyzed by different chemical species such as inorganic and organic mediators (Fe2+ and Polypirrole, respectively (49)). Abiotic oxygen reduction may result from different pathways (50): according to a single step, in four-electron mechanism (reaction 1), or two successive electron reduction steps according to reactions 2 and 3, that is, with the intermediate formation of hydrogen peroxide (51, 52) as follows: +
O2 + 2e- f 2H + H2O2 -
+
H2O2 + 2e f 2H + 2H2O
(2) (3)
The oxygen reduction mechanism on SS surfaces is strongly influenced by biofilms (53). In fact, prior to the formation of a biofilm, oxygen reduction occurs in a single step (reaction 1). After a while, the biofilm grows on the metal surface and Ecorr ennobles to positive values. On the basis of cathodic polarization tests, Shams El Din et al. (53) postulated that once the biofilm settles, oxygen reduction occurs in two successive electron-reduction steps (reactions 2 and 3). Significant concentrations of H2O2 were detected as a result of the reduction of oxygen on metals immersed in seawater (54, 55). Electrochemical tests combined with XPS (X-ray photoelectron spectroscopy) analysis allowed to show the important role played by SS passive films on oxygen reduction in natural seawater (56). MIC studies evidencing the oxygen reduction catalyzed by biofilms have been performed using the most common electrochemical techniques (57): (i) by registering dynamic cathodic polarization curves after Ecorr ennoblement, starting either from Ecorr value or from an anodic potential; (ii) by registering cathodic current as a function of immersion time in potentiostatic tests at the potential range where oxygen may be reduced. However, such techniques do not provide an explanation for the fine oxygen reduction mechanism catalyzed by biofilms. More local approaches are needed to obtain accurate data about the evolution of cathodic active sites on metal surfaces. To this end, Mollica et al. (58) used the scanning vibrating electrode technique (SVET). Their results showed that the marine biofilm generates a current increase of 2 orders of magnitude, although only 2% of the surface was occupied by cathodic sites where oxygen could be reduced.
TABLE 1. Enzymes from Biofilms Inhibited by Azide and the Corresponding Mechanism of Inhibition (C, Competitive; IR, Irreversible; R, Reversible) (61) adenosintriphosphatase anthranilate 2,3 dioxygenase l-ascorbate peroxidase bile-salt sulfotransferase carbonate dehydratase catalase cellobiose oxidase CMP-N-acetylneuraminate-lactosylceramide R-2,3 sialyltransferase cyclohexanone monooxygenase ferredoxin-nitrite reductase formate dehydrogenase galactose oxidase glycerol oxidase hexose oxidase H+-transporting ATP synthase hydroxylamine dismutase lignine peroxidase mannotetraose 2-R-n-acetylglucosaminyltransferase monophenol monooxygenase myeloperoxidase peroxidase superoxide dismutase tryptophan 2,3-dioxygenase
R R C R R R R R R R R R C R R R IR R R R R R R
3.1.2. Enzyme-Influenced Oxygen Reduction. The reduction of oxygen is considered as the driving force in aerobic corrosion. The development of a biofilm on SS surfaces modifies the oxygen reduction wave: a displacement toward anodic values (between 0 and +300 mV/SCE) and an increase of the current density (3, 4, 11, 23, 36, 53, 59, 60). Scotto et al. (3) and Mollica (60) suggested that one of the ways by which biofilm formation may favor these phenomena is through enzymatic catalysis. The use of sodium azide on natural biofilms provoked the inhibition of enzymes with the consequent death of most microorganisms (61). Under these conditions, Ecorr decreased markedly and then increased afterward when the inhibitor was removed from the solution. The authors concluded that the ennoblement is a reversible phenomenon, reflecting the reversibility of azide inhibiting action on most of the enzymes (Table 1), in spite of the microorganism death. The influence of enzymes has been recently investigated (62, 63): peroxidase (EC 1.11.1.7) and catalase (EC 1.11.1.6) are of particular concern, as they have been detected in some marine biofilms (64). All these proteins possess a heme-group VOL. 42, NO. 7, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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(also called hemins) which is involved in the transfer of electrons during the enzymatic catalysis. When hemin alone was used in local electrochemical tests using SVET, the cathodic behavior of the hemin-coated area and the anodic behavior of the bare area of the SS surface were confirmed (62). Hemin alone has no enzymatic activity, but it proved its ability to shift Ecorr toward anodic values when immobilized on an SS surface (62). Therefore, in proteins with no enzymatic activities, the presence of hemin is sufficient to enhance oxygen reduction on SS surfaces. For example, myoglobin, a protein with no enzymatic activity, was able to provoke oxygen reduction catalysis on a carbon electrode (63). In conclusion, biofilm proteins that are able to enhance oxygen reduction will have to (i) be excreted by cells and (ii) have an electroactive moiety, essentially the heme-group with facultative enzymatic activity. 3.1.3. Pivotal Role of Hydrogen Peroxide (H2O2). Biofilms formed in natural seawaters are able to generate hydrogen peroxide (H2O2) (45, 65–67), one of the reactive intermediates of oxygen reduction (Figure 4). The H2O2 concentration within the biofilm, estimated to be in the range of mmol/L, is governed by two antagonist processes: the production by some oxidases (enzymes using O2 as electron acceptor) and the simultaneous degradation by enzymes which protect microorganisms against oxidative stress (catalases, peroxidases). In fact, many bacteria release hydrogen peroxide as the end product of oxygen reduction and contribute to the steady level of H2O2 in seawater (66, 68–70). From the electrochemical point of view, H2O2 is a common oxidant (reaction 3) which exhibits a very high standard potential (E° ) 1.77 V/SHE). Because of its redox potential higher than that of oxygen, H2O2 plays an important role in the ennoblement of SS in natural waters (5, 7, 71–75). A direct correlation between Ecorr values and hydrogen peroxide concentration was evidenced on AISI 316L SS in natural seawater (74). In these experiments, H2O2-decomposing enzymes (catalase and peroxidase) were added and an offset of Ecorr ennoblement was obtained. By contrast with many authors’ opinion, Salvago and Magagnin (49) consider that H2O2 does not play a direct role in the Ecorr ennoblement, especially in the case of SS with Ecorr higher than 100 mV/SCE. Indeed, H2O2 is not stable thermodynamically at potentials ranging from 100 to 850 mV/SCE (76). Moreover, ferrous and ferric compounds are able to catalyze H2O2 decomposition (77, 78). Finally, even if the direct role of H2O2 in the Ecorr ennoblement is controversial, this oxidant is at the crossroad of many enzymatic reactions involved in aerobic MIC mechanisms. 3.1.3.1. Enzymes Decomposing H2O2: Catalases. Catalases enzymes are present in all aerobic microorganisms. They catalyze the decomposition of H2O2 to form oxygen and water: 1 H2O2 f O2 + H2O 2
(4)
The enzyme is usually intracellular but some secreted forms are inducible in response to oxidative stress (79). As depicted in Figure 5, the activity of catalases generates O2 which can be used to produce H2O2 again by reduction on SS surface. This “autocatalytic mechanism” was first proposed by Busalman et al. (80, 81). By using cultures of Pseudomonas sp., which secrete catalases, they have observed an increase in the cathodic current. Lai and Bergel (82, 83) confirmed this mechanism with electrochemical tests using a purified enzyme. Different methods were compared to introduce the enzyme (i) free in the electrolyte, (ii) immobilized in a glutaraldehyde-modified electrode, (iii) entrapped in a Nafion-modified electrode, and (iv) adsorbed on a dimethylsulfoxide (DMSO)-modified electrode. For all these conditions, cathodic polarization tests 2236
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FIGURE 5. Proposition of enzymatic mechanisms in aerobic MIC: (I) production of H2O2, (II) degradation of H2O2, and (III) degradation of H2O2 with O2 recycling. Enzymatic reactions are indicated with dotted lines. showed that oxygen reduction occurred in two successive two-electron reactions (reactions 2 and 3). When catalase activity is present near the surface, a part of the H2O2 produced electrochemically (reaction 2) is transformed enzymatically into O2 (Figure 5, mechanism I, “H2O2 disproportionation”). This newly formed oxygen may then be reduced on the electrode according to reaction 2. Therefore, the recycling reaction yielding O2 induces a cathodic current increase (82). Furthermore, the authors postulated that a direct electron transfer from the electrode to catalase is possible and results in oxygen reduction (reaction 1) (83). 3.1.3.2. Enzymes Producing H2O2: Oxidases. Actually, the involvement of oxidases is an hypothesis which was endorsed not only by the formation of H2O2 in the biofilm, but also by investigations of the probable connections between biofilm growth and Ecorr ennoblement. Contrary to previous observations (61), Dupont et al. (21) suggested that EPS (exopolysaccharides) alone were not able to reproduce the electrochemical effect of biofilms. This conclusion was obtained experimentally by monitoring Ecorr at two different temperatures: 25 and 40 °C. Their results showed that ennoblement occurred at 25 °C but not at 40 °C although the quantity of EPS and microorganisms was kept constant at both temperatures. However, the taxonomy differed: at 25 °C, the bacteria present in the biofilm secrete enzymes that catalyze sugar degradation, accompanied by H2O2 production, suggesting the involvement of oxidases. By contrast, these catalytic activities were not found at 40 °C. Generally, glucose molecules may be detected in a significant amount in biofilms formed on SS surfaces (84). As a consequence, glucose oxidase (E.C. 1.1.3.4) was thoroughly studied in electrochemical tests (6, 7, 71, 85). This enzyme catalyzes the oxidation of glucose to form gluconic acid and H2O2 according to reaction 5. C6H12O6 + O2 + H2O f C6H12O7 + H2O2
(5)
In the experiments performed by Amaya et al. (6), a new enzyme-based method was established to test the corrosion behavior of SS in seawater. By using a purified glucose oxidase in the presence of glucose in sterile seawater, electrochemical experiments reproduced Ecorr ennoblement and the cathodic current increase. Amaya et al. (6, 7, 86) and Dupont et al. (71) proposed an enzymatic model based on the formation of H2O2 according to the mechanism II depicted in Figure 5. In the first stages of the immersion, prior to microbial adhesion, macromolecules are adsorbed on the SS surface by an irreversible mechanism yielding a “conditioning film” (87). These substances are then oxidized by some microbial
and manganese oxides deposition. However, these authors disagreed on the stoichiometry of the reaction (reactions 6 and 7). Adams et al. (100) analyzed the Mn deposits produced by L. discophora SS-1. They found that the oxidation state of Mn was ranging from 3.32 to 3.62 and varied with the oxide aging. Oleson et al. (101) used XPS to identify Mn oxides. For this purpose, the authors artificially deposited Mn dioxide on SS samples and they reduced it electrochemically. Their results showed that Mn dioxide deposits were reduced to Mn2+ by using two electrons from the metal. In addition, MnOOH was identified as an unstable intermediate of this reaction. Thus, the authors proposed a mechanism based on reaction 7 followed by: FIGURE 6. MIC mechanism of stainless steel by biomineralized manganese oxides (95). metabolic processes, the foremost of which are the reactions catalyzed by oxidases immobilized in the biofilm matrix. Recently, Féron et al. (88) proposed a model called “biochemical artificial seawater” to perform reproducible corrosion tests on SS (crevice or pit corrosion). This model was composed of glucose oxidase and glucose in artificial seawater. 3.1.4. Microbial-Induced Deposition of Mn Oxides. Many authors have established a correlation between microbial deposition of Fe and Mn oxides, or hydroxides, and Ecorr ennoblement. Mn biomineralization hypothesis is much more documented (16, 89–95). The presence of Mn oxides/ hydroxides in biofilms was reported to be responsible for pitting corrosion of SS exposed to natural waters (96–98). The formation of Mn oxide deposits on AISI 316L samples was observed after 35 days of immersion in natural fresh water. These deposits were attributed to Mn oxidizing bacterial colonies. The authors confirmed this result by exposing SS samples to a pure culture of Mn oxidizingbacteria, Leptothrix discophora SP-6, in a medium containing divalent Mn. By using EDX and X-ray diffraction analysis, a significant amount of Mn oxyhydroxide and Mn dioxide was evidenced on corroded samples in low chloride medium (89, 90). According to these experiments, Ecorr ennoblement is caused by the presence of Mn dioxide as described by the following reaction (6): MnO2(s) + 4H+ + 2e- f Mn2+ + 2H2O E ° ) + 1.28 V/SCE (6) In fresh water, Dickinson et al. (16, 91) observed a correlation between the ennoblement on SS samples and the surface coverage by a thin film of hydrous Mn dioxide. According to these authors, the electrochemical behavior observed in this case can be described by the following reaction: MnO2(s) + H+ + e- f MnOOH(s)
E ° ) + 0.81 V/SCE (7)
Figure 6 summarizes the mechanism proposed by Dickinson et al. (91). The ennoblement induced by Mn oxides is of particular interest for corrosion researchers because the Ecorr values obtained in natural media are near the equilibrium potential of Mn oxides. According to reaction 6, Ecorr is determined by the MnII/MnIV ratio. The redox potential calculated at pH ) 7 and with [Mn2+] ) 0.1 mg/L is equal to +327 mV/SCE (98). This value corresponds well to the Ecorr found in natural media (99). In natural rivers (pH∼8), the final Ecorr value obtained was about +350 mV/SCE (16); this is in agreement with the reduction potential value of reaction 7 (+335 mV/SCE). In both previous studies, Linhardt (89, 90) and Dickinson et al. (16, 91) proved the connection between ennoblement
MnOOH(s) + 3H+ + e- f Mn2+ + 2H2O E ° ) + 1.26 V/SCE (8) Thus, MnO2 is formed from Mn2+ by Mn oxidizing bacteria, and then it is reduced according to reactions 7 and 8. In all these approaches, we can highlight two important points: (i) the reduction of Mn oxides is a cathodic reaction which can be summed to the oxygen one, and therefore it explains Ecorr ennoblement according to Figure 3a; (ii) the electrochemical effect observed in the presence of Mn oxidizing bacteria requires a direct contact between Mn oxides/hydroxides and the SS surface. Because of the low growth rate of manganeseoxidizing bacteria, they are easily removed from the SS surface by other microorganisms (102). When this competition occurs, the contact between manganese-oxidizing bacteria and SS surface is lost and the deposition of MnO2 (Figure 5) is no longer possible. It is well-known that MnII-oxidizing microorganisms, primarily bacteria and fungi, accelerate the rate of Mn biomineralization (103, 104). Besides oxygen, Mn oxides are some of the strongest naturally occurring oxidizing agents in the environment, and they participate to numerous redox and interfacial reactions. They also serve as terminal electron acceptors for bacterial respiration (105). Actually, these bacteria produce an extracellular protein responsible for the Mn ion oxidation. Adams et al. (106) demonstrated that the oxidizing activity of Leptothrix discophora SS-1 needs specific conditions (optimal temperature and pH) which suggest that it can be due to an enzymatic activity. The same authors isolated a protein of approximately 100000 MW from Leptothrix discophora SS-1 cells which was responsible, at least partly, for the Mn oxidizing activity (106). The biochemical mechanism of MnII oxidation has not been described yet because neither native purification nor heterologous overexpression of putative MnII oxidases has been successful to date (105). However, numerous details of a regulated functional pathway have been reported. Multicopper oxidase (MCO)-type enzymes have an integral role in MnII oxidation in various species. Genetic studies indicate that the site of MnII oxidation is likely to be at the cell surface, thus reinforcing the need of a direct contact with the SS surface. MCO is a family of enzymes characterized by conserved Cu-binding sites and a catalytic mechanism involving a sequential one-electron oxidation of the substrate with the concomitant reduction of O2 to H2O. Genes encoding an MCO with MnII oxidase activity were found in Bacillus sp. SG-1, Pseudomonas putida MnB1 and GB-1, and L. discophora SS1 (105). For fungi, the mechanism of the Mn oxide deposition is unknown but it is likely to be similar to the one occurring in bacteria. Both fresh water and marine systems contain fungal Mn oxide producers. Similarly to the findings concerning L. discophora SS-1, an extracellular protein was shown to be involved in Mn oxide formation (107, 108). These studies showed that the Mn-oxidizing protein can also oxidize some of the known substrates of laccases such as p-phenyleneVOL. 42, NO. 7, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 7. Possible mechanisms explaining cathodic depolarization (150). diamine and 2,20-azinobis(3-ethylbenzothiazoline-6-sulfonic acid). Purified laccases from Trametes versicolor (109) and Stropharia rugosoannulata (110) were shown to be able to oxidize MnII to form MnIII. Fungi can also oxidize MnII with the help of heme-containing Mn peroxidases involved in the degradation of lignin. Furthermore, in the presence of a suitable MnIII chelator, MnII can be oxidized to MnIII by a peroxide-oxidizing enzyme from fungi (105). Thus, it is important to note that in the Mn oxidizing processes, two enzymes can be identified: fungal laccase oxidizes MnII to MnIII directly (110) and manganese peroxidase oxidizes MnII to MnIII in the presence of H2O2 (111). Accordingly, manganese peroxidase (EC 1.11.1.13) catalyzes the following reaction (112): 2Mn(II) + 2H+ + H2O2 f 2Mn(III) + H2O
(9)
Finally, the intermediate formation of MnIII required during the microbial-induced oxidation of MnII to MnIV (113, 114) suggests the involvement of the enzymatic pathways described above. 3.2. Mechanisms in Anaerobic MIC. A significant part of microbial activities in biofilms is due to anaerobic microorganisms (115). Interactions between these microorganisms and the SS passive layer are not well defined because of the complexity of the passive layer/biofilm interface. Some obligate or facultative anaerobic bacteria use metal oxides as the terminal electron acceptor in neutral pH environment (116, 117). Many authors have observed a correlation between the direct contact with some bacteria and the reduction of Fe2O3 and FeIII, thus indicating an enzymatic influence (118–121). Geobacter sulfurreducens and G. metallireducens are both able to reduce ferric oxides with simultaneous oxidation of dihydrogen and organic acids (119, 120). Furthermore, these anaerobic bacteria reduce the metal ions via their cytochrome c-utilizing enzymes that are preferentially located on the outside surface of the bacterial cell membrane (119, 120). Hence, these reactions with iron, influenced by G. sulfurreducens and G. metallireducens, are likely to be able to accelerate the cathodic reaction. However, no direct evidence was published to date. Other anaerobic microorganisms were unambiguously associated with corrosion process. Sulfate-reducing bacteria (SRB) and thiosulfate reducing-bacteria (TRB) are the most important bacteria causing degradation of metals and alloys by amplifying the cathodic reaction (122–124). These bacteria can reduce sulfate to sulfite ions which precipitate with ferrous ions to form iron sulfides (FeSx). These insoluble biogenic products were recently observed on SS samples (125). They act as a cathode in a galvanic couple with steel, thus enhancing corrosion (126, 127). Alternatively, the 2238
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reductive dissolution of iron oxides can be promoted by the formation of surface complexes. This mechanism was evidenced by using experiments in media containing H2S and organic sulfides (cysteine) (128, 129). Some of the proteins secreted by SRB correspond to key enzymes in MIC (130–134): (i) hydrogenases (EC 1.12.1.2); (ii) adenosine 5′-phosphosulfate (APS) reductase (EC 1.8.99.2), the key enzyme of the dissimilatory sulfate respiration, converts the activated form of sulfate into sulfite and AMP (134); (iii) sulfite reductase (EC 1.8.1.2) catalyzes the sixelectron reduction of sulfite yielding sulfide, and it is also involved in sulfate respiration. It has been purified and characterized from anaerobic bacteria involved in MIC (135–137). To date, only hydrogenases were studied in electrochemical tests on SS. There is compelling evidence suggesting their direct involvement in corrosion (138–142). However, it is still matter of debate because some SRB strains can provoke a high corrosion rate even without possessing hydrogenase activities (143–145). Hydrogenases are involved in the metabolism of many anaerobic bacteria and they catalyze the reversible reduction of protons (reaction 10). 2H+ + 2e- T H2
(10)
Some authors (142, 147, 148) suggested that hydrogenases consume molecular hydrogen and shift the equilibrium of reaction 10 toward the consumption of protons. This hypothesis was reported as “cathodic depolarization”. Nowadays, it is well established that corrosion is a kinetically controlled process which is globally irreversible (149). Therefore, it seems unlikely that the enzymatic consumption of hydrogen affects directly the cathodic kinetics, so this hypothesis was abandoned. The question about a direct interaction between hydrogenases and the metal surface is still a source of debate. Indeed, a direct contact with SRB was necessary to increase the corrosion rate of carbon steel (141). Recently, Da Silva et al. (150, 151) have studied the electrochemical behavior of AISI 316L SS in the presence of a NAD-dependent hydrogenase in phosphate buffer medium (pH 8.0). These authors investigated the electron transfer between the enzyme and the SS and its consequence on the cathodic response of the metal. They have observed an increase of the cathodic current in the presence of NAD-dependent hydrogenase and proposed three possible mechanisms (Figure 7) to explain this phenomenon (150): (Mechanism A) Protons are reduced electrochemically on SS surface. NAD-dependent hydrogenase consumes the hydrogen produced on the metal and enhances the reduction rate by regenerating one proton
and a molecule of NADH. (Mechanism B) It corresponds to a direct electron transfer between NAD-dependent hydrogenases and the SS. The NAD-dependent hydrogenase catalyzes the transformation of NAD+ and H+ into (NADH + H+) with 2 e- transferred from the SS. This mechanism suggests a direct contact between the enzyme and the SS surface. (Mechanism C) This mechanism is also based on an electron transfer between hydrogenase and SS. However, there is no direct contact between the surface and the enzyme: the electron transfer occurs via adsorbed intermediate species of hydrogen. The necessity of a direct contact between SRB cells or hydrogenases was also investigated by other authors (152–154). Their experiments consist in totally separating steel samples and SRB or hydrogenases in two bottles connected only through the common gas phase. Results showed a significant increase of the corrosion rate. These results are very intriguing because they suggest a consumption of molecular hydrogen from the gas phase. In fact, while hydrogen evolution is an irreversible process, a depletion of H2 in the gas phase cannot have any effect on the hydrogen evolution rate. Da Silva et al. have given a likely explanation for these results: the authors postulated that phosphate species used in different experiments are involved in the cathodic processes (155). Recently, a linear correlation between reduction waves in linear voltammetry, in the presence of hydrogenases, and phosphate concentration at a constant pH value has been established (156). Indeed, the reaction which enhances the production of dihydrogen is the following: 21 H2PO4 + e f HPO4 + ⁄2H2
(11)
According to the mechanism proposed by these authors, called “phosphate deprotonation”, the consumption of H2 by SRB or free hydrogenases causes the equilibrium of reaction 11 to shift and thus enhancing the cathodic reaction rate (156). Besides the cathodic influence described above, hydrogenases may also induce a protective effect against corrosion involving phosphate species (157). Furthermore, some highly corrosive P-compounds produced by SRB cause a significant increase in the corrosion rate of steel (158). Both effects were only observed on carbon steels but may constitute an interesting issue in anaerobic MIC researches for SS.
4. Prospects In the present review, aerobic and anaerobic enzymeinfluenced mechanisms were identified: (i) a unified enzymatic model involving the oxygen reduction is proposed (Figure 5). (ii) In anaerobic MIC, hydrogenases are of particular interest because of their catalytic ability toward the H2 consumption. In both cases, the increase of the cathodic reaction rate induced by enzymes could occur only in a restricted range of redox potential inside biofilms which may explain why, fortunately, MIC does not always occur when bacteria are present on metallic materials. To conclude, all the identified enzymes responsible for MIC of SS belong to the class of oxidoreductases. Their ability to exchange electrons seems to be crucial for their involvement in MIC. According to the literature, enzymes can be useful to model MIC even if some improvements are still needed. Indeed, biofilms correspond to a gel matrix with embedded enzymes. This suggests that there must be a natural limitation of the diffusion rates of substrates and products. Consequently, it appears that the best biomimetic system would be a polymer film coreticulated with enzymes and in contact with the SS surface. This biomimetic film will
reproduce the discrete concentrations in electroactive species at the SS surface as well reproduce the hindering of some SS active sites. In a pioneering study, Landoulsi et al. (159) have proved the efficiency of such an approach for the determination of physicochemical and enzymatic factors influencing MIC. Such experiments of heterogeneous enzymology may pave the way to new comprehensive approaches to understand MIC.
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