Corrosion characteristics of sulfate-reducing bacteria (SRB) and the role of molecular biology in SRB studies: an overview
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Balakrishnan Anandkumar
Balakrishnan Anandkumar holds an MSc in Microbiology, and a PhD in Chemistry and he has two years of post doctoral experience as a visiting scientist at IGCAR, Kalpakkam, India. He has more than 11 years of research experience in microbiologically influenced corrosion and biofilm control. His interests are the development of molecular biological tools for the identification of microbial groups involved in biofouling of titanium condenser tubes and biofouling control techniques. He has 28 journal papers and 15 conference proceedings in the fields of biofilms and microbial corrosion.
Rani P. George holds an MSc in Botany and a PhD in Botany and having spent two years as a visiting scientist in IGCAR, Kalpakkam, India. She also worked as a Visiting Scientist at Corrosion Protection Centre, UMIST, Manchester, UK during 1998 in the field of MIC probes. She has authored more than 60 journal papers and 30 conference proceedings in the fields of biofouling and corrosion. She has spent 20 years in the field of biofilms and involved in the development of corrosion and biofouling resistant coatings on titanium, stainless steel, low chromium alloys for seawater and humid coastal atmospheric applications.
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Sundaram Maruthamuthu
Sundaram Maruthamuthu holds a Master’s degree and a PhD in Marine Biology. He had worked as a visiting scientist in Dexter, US and as a Brain Pool fellow in South Korea (2012). He has spent 22 years in the fields of Microbial Corrosion and Bioelectro Kinetics, Passivation of stainless steels, Microbial corrosion in petroleum industry, Cathodic protection and microfouling. He has published more than 100 research papers and 50 conference papers. He has completed and also has many organizations sponsored research projects to his credit.
Natarajan Parvathavarthini holds an MSc in Chemistry, an MS in Metallurgical Engineering, and a PhD in Metallurgy. She was a visiting scientist at the Technical Management Concepts, Inc., Wright Patterson Air Force Base, Ohio, USA (1996–1997). She has spent 38 years in the field of localized corrosion such as pitting, crevice, IGC, and hydrogen embrittlement of nuclear structural materials. She has published 121 research papers and 23 design notes for fast reactors.
Uthandi Kamachi Mudali holds an MSc in Materials Science, an MTech in Corrosion Science and Engineering, and a PhD in Metallurgical Engineering. He is a fellow of several international and national societies like NACE International, ASM International, and honorary fellow of the Electrochemical Society of India, etc. He has made excellent contributions to materials development and corrosion control of reactor and reprocessing materials in nuclear industry. He has published 371 papers in journals, co-edited 14 books/proceedings, and holds an H-index of 24. He has guided/coordinated project works of 142 students for their undergraduate, postgraduate, and PhD degrees. He is a Professor at Homi Bhabha National Institute University and an Adjunct Professor at the PSG Institute of Advanced Studies, Coimbatore.
Abstract
Sulfate-reducing bacteria (SRB), an anaerobic bacterial group, are found in many environments like freshwater, marine sediments, agricultural soil, and oil wells where sulfate is present. SRB derives energy from electron donors such as sulfate, elemental sulfur or metals, and fermenting nitrate. It is the major bacterial group involved in the microbiologically influenced corrosion (MIC), souring, and biofouling problems in oil-gas-producing facilities as well as transporting and storage facilities. SRB utilizes sulfate ions as an electron acceptor and produce H2S, which is an agent of corrosion, causing severe economic damages. Various theories have been proposed on the direct involvement of H2S and iron sulfides in corrosion; H2S directly attacks and causes corrosion of metals and alloys. Many reviews have been presented on the aforementioned aspects. This review specifically focused on SRB corrosion and the role of molecular biology tools in SRB corrosion studies viz. cathodic and anodic depolarization theories, corrosion characteristics of thermophilic SRB and influence of hydrogenase, temperature, and pressure in thermophilic SRB corrosion, SRB taxonomy, molecular approaches adopted in SRB taxonomical studies, sulfate and citrate metabolism analyses in completed SRB genomes, and comparative studies on SRB’s dissimilatory sulfite reductase structures.
1 Introduction
Sulfate-reducing bacteria (SRB) play many roles in the various environments, like involvement in the sulfur cycle, heavy metal degradation, and anaerobic corrosion of different materials. SRB were mostly recognized as the main culprit in the production of H2S, within reservoirs, which reduces oil quality, corrodes steel material, and threatens workers’ health due to its high toxicity (Cord-Ruwisch, Kleinitz, & Widdel, 1987). Molecular approaches and technologies like next-generation sequencing and microarrays are leading scientists to explore many aspects of SRB in different environments. The biotechnological aspects of SRB have been reviewed by Muyzer and Stams (2008) and Meulepas, Stams, and Lens (2010). The involvement of SRB in corrosion in different environments has been reported and reviewed by many researchers for more than five decades (Lee, Lewandowski, Nielsen, & Hamilton, 1995; Malard, Kervadec, Gil, Lefevre, & Malard, 2008; Halim, Watkin, & Gubner, 2012; Li, Whitfield, Krystyn, & Van Vliet, 2013). However, SRB corrosion at high temperatures is reported only by few workers (Villanueva, Martinez, Dlaz, Martinez, & Sanchez, 2006; Anandkumar, Choi, Venkatachari, & Maruthamuthu, 2009a; Anandkumar, Rajasekar, Choi, & Maruthamuthu, 2009b). Microbiologically influenced corrosion (MIC), as an interdisciplinary subject and mechanism, can only be elucidated through chemistry, microbiology, and molecular biology. An overview on SRB taxonomy, physiology, and habitats of thermophilic SRB and theories supporting the corrosion by thermophilic SRB are presented in this article. This review article also highlights the role of molecular biology tools in SRB studies.
2 Corrosion mechanisms of SRB
Microbial corrosion results from the presence of biofilm, which can influence local chemistry near the metal surface. The biofilm consists of three compartments: bulk fluid, biofilm, and substratum. Biofilm accumulation is a dynamic process, and as the water chemistry at the interface between the metal and the biofilm changes with time, corrosion is initiated. Thus, microbial corrosion is the net result of the interaction between various compartments, which are in dynamic flux.
A logical mechanism for corrosion caused by sulfate reducers was first provided by the classical theory of von Wolzogen Kuhr (1961), which proposed the following sequence of events as the mechanism of anaerobic bacterial corrosion:
Anodic reaction:
Dissociation/ionization of water:
Cathodic reaction:
Cathodic depolarization by SRB:
Corrosion products:
Overall reaction:
von Wolzogen Kuhr and van der Vlugt (1934) claimed that the cathode is depolarized by the metal oxidation of hydrogen by SRB for its characteristic sulfate reduction process. The proposal was supported by an earlier observation that SRB releases the enzyme hydrogenase, which is the removal of hydrogen for the reduction of sulfate. SRB oxidize the molecular hydrogen, which prevents the polarization of the cathode, leading to cathodic depolarization [Equation (4)], and the reaction of sulfide (HS-) ions with ferrous ions, producing iron sulfide, which is cathodic to steel, enhances corrosion again through cathodic depolarization (Smith & Miller, 1975). Thus, SRB enhances the corrosion of steel through direct (hydrogen removal) and indirect (hydrogen sulfide and iron sulfide production) processes. The importance of dissolved oxygen (DO) in SRB-influenced corrosion of ferrous metals and alloys has been emphasized by many authors (Hardy & Bown, 1984; Hamilton, 1990; Moosavi, Pirrie, & Hamilton, 1990). Further, many researchers focused on (i) corrosion by mild steel underneath aerobic biofilm containing SRB at low oxygen niches (Lee, Lewandowski, Okabe, Characklis, & Avci, 1993a), (ii) iron corrosion by anaerobic microbes (Dinh et al., 2004), (iii) interactions between steels and sulfide-producing bacteria in corrosion of steels (Malard et al., 2008), (iv) corrosion by halophilic hydrogenotrophic SRB Desulfovibrio gabonensis and Desulfovibrio capillatus due to gradient concentrations of hydrogen ion species formed in the solution within the metal-biofilm interface (Castaneda & Benetton, 2008) and the role of direct microbial electron transfer in the corrosion of steels (Mehanna, Basseguy, Delia, & Bergel, 2009).
Subsequent investigations on the role of different types of sulfides and extracellular polymeric substances (EPS) on steel were reported. Within the biofilms, EPS plays different roles like conditioning of the substratum, helping in food transport, accumulation of metal ions, and, rarely, mitigation of corrosion. Corrosion and corrosion mitigation by Pseudomonas sp. have been well discussed (Abdolahi, Hamzah, Ibrahim, & Hashim, 2014). Sun, Xu, and Wang (2011) explained SRB corrosion caused by EPS and other compounds more than the involvement of sulfide in the corrosion of steels. Anaerobic corrosion of carbon steel by SRB Desulfovibrio desulfuricans was well explained in five stages (Sun et al., 2011) as deposition of oxides and phosphorus compounds, giving cell protection from harmful substances such as free oxygen in the first stage, large accumulation of SRB cells causing desorption of phosphorous compounds and oxides creating anoxic zone in the second stage, production of EPS by SRB in the third stage, exfoliation of biofilms and decline in the SRB cell numbers in the fourth stage, and redeposition of phosphorous compounds and increase in the steel surface pH due to small amounts of Ca(OH)2 in the fifth stage.
Enning and Garrelfs (2014) have reviewed the SRB corrosion of iron in anoxic conditions with two possible mechanisms based on dissimilatory sulfate reduction and electrons withdrawal. The latter mechanism based on electrons withdrawal has been discussed in Section 2.3.
2.1 Anodic depolarization
SRB corrosion due to anodic depolarization was reported by Salvarezza and Videla (1986), Daumas, Cord-Ruwisch, and Garcia (1988), and Crolet (1992). Hamilton and Lee (1995) hypothesized the localized acidification of the anode (anodic depolarization) resulting from the formation of ferrous sulfide corrosion products (Crolet, 1992; Daumas et al., 1988) as given in Equation (8).
SRB biofilms initiate the anodic corrosion process. The overall anodic corrosion process should be the result of passivation and activation process that are taking place at the same time on the metal surface (Villanueva et al., 2006). The organic metabolites of acetate and lactate may act as anodic inhibitor, which reduces anodic current in the presence of thermophilic SRB isolates, as acetate metabolism is incomplete when compared to propionate. The complete oxidation of propionate in mesophilic SRB strains contributes to anodic depolarization. As the formation of iron sulfide is cathodic to the parent metal, mesophilic Desulfobulbus propionicus enhances anodic current, thereby increasing corrosion (Anandkumar, George, Maruthamuthu, Palaniswamy, & Dayal, 2010).
Miranda et al. (2005) reported corrosion in carbon steel by D. capillatus and observed marked decrements in the potential, finally reaching a stable corrosion potential (Ecorr). The decrement in potentials could have resulted from the establishment of a biofilm, metabolic processes associated with microbial colonization and growth, and establishment of a cathodic reaction in which the reversible potential was low. They also noticed high corrosion current in the presence of bacteria. They explained that sulfides or some other metabolic product of bacteria had accelerated the anodic reaction.
2.2 Cathodic depolarization
The cathodic depolarization theory proposed by von Wolzogen Kühr and van der Vlugt (1934) as given in Equations (1) to (7) was evidenced in both mesophilic and thermophilic SRB-influenced corrosion by many investigators (Villanueva et al., 2006; Anandkumar et al., 2009a; Anandkumar et al., 2009b). The thermophilic strain survive a temperature range of 50°C–80°C by forming spores, and their vegetative forms might develop and multiply when the optimum temperature for growth is encountered. The organic film adsorbed on the metal surface reduces the anodic current where the biogenic product may improve the passivity of steel (Anandkumar et al., 2009a; Anandkumar et al., 2009b). Although passivity was noticed on the steel, it is assumed that the heterogeneity of bacterial attachment and temperature encourages the pitting corrosion on the metal surface. SRB degrade organic substances to CO2, promoting the formation of siderites, and oxidize hydrogen. The removal of hydrogen leads to the depolarization of cathode, which enhances uniform corrosion attack (Postgate, 1984). Bryant and Laishley (1990) reported that hydrogenase localized inside SRB and exocellular hydrogenase entrapped in the biofilm could induce a cathodic depolarization phenomenon. This phenomenon was also noticed in the corrosion of low alloy steels by Desulfotomaculum species where anodic process was slowed down due to accumulated iron sulfides (Cetin & Aksu, 2009).
The involvement of hydrogenases in cathodic depolarization, which are either present in bacteria or free in solution, remains a controversial subject. Bryant, Jansen, Boivin, Laishley, and Costerton (1991) have demonstrated that there is a direct correlation between the presence of hydrogenase in SRB and corrosion. Rameshkumar, Singh, and Nigam (1999) claimed that a hydrogenase-negative strain of SRB was more corrosive than hydrogenase-positive strains. Mehanna et al. (2008) monitored the free potential of single coupons exposed to the hydrogenase in a classical cell. They concluded that [Fe]-hydrogenase catalyzes direct proton reduction on the mild steel surface in the absence of any final electron acceptor after a complete deoxygenation.
Various mechanisms on solvent reduction catalysis were reported by da Silva, Basseguy, and Bergel (2002). The proton (or solvent in alkaline media) is reduced electrochemically, and hydrogenase consumes the hydrogen produced and thus enhances the reduction rate. This mechanism exactly corresponds to the so-called theory of cathodic depolarization. However, this mechanism has severely been criticized. The most likely mechanism should consequently be a direct electron transfer between hydrogenase and steel. In another mechanism, it is stated that hydrogenase is adsorbed directly on the steel or the electron transfer occurs via unadsorbed intermediate species of hydrogen. The enhancement of the charges exchanged should correspond to a cathodic depolarization, which occurs through the direct electron transfer from stainless steel to hydrogenase. Mehanna et al. (2008) explained two mechanisms for the involvement of hydrogenase in corrosion of steels: (i) a reversible reaction based on the cathodic deprotonation of phosphate species and corrosion accelerated due to the dihydrogen consumption catalyzed by hydrogenase and (ii) the direct catalysis of proton/solvent reduction by adsorbed hydrogenase.
2.3 The influence of HS, iron sulfides, ferrous ion, organic content, and O2 activity in SRB corrosion
An increase in anaerobic corrosion of iron with the addition of ferrous ions was reported by Lee and Characklis (1993). Lee et al. (1993b) reported that if the concentration of ferrous ion is low, corrosion current densities are low due to adherent and temporary iron sulfides film. Iron sulfide film formed in low iron media acts as a protective coating under the biofilm. This is not formed in iron-rich media, and therefore, corrosion current densities increased. This effect is due to the reaction of ferrous ions with the free H2S, which prevente the formation of iron sulfide film, thus allowing the cells to come in contact with the iron surface, as in the depolarization theory. Considerable work has been centered on the influence of ferrous ions on SRB action on the steel alloys. Breakdown of the passive film of the steel was induced by iron sulfide in acidic pH, which leads to the formation of electrochemical cells with steel as the anode (Hamilton, 2003; Kakooei, Ismail, & Ariwahjoedi, 2012). Obuekwe, Westlake, Cook, and Costerton (1981) reported extensive pitting of mild steel when ferrous and sulfide ions were being formed concurrently. If only sulfide was produced, corrosion rates first increased and then declined due to the formation of a protective FeS film. The high levels of soluble iron prevented the formation of such protective layers, leading to high corrosion rates. Kakooei et al. (2012) have reviewed the influence of iron sulfide in SRB corrosion through various mechanisms. Another study by Wikieł, Datsenko, Vera, and Sand (2014) also reported the increase in corrosion rates after the production of sulfide and decrease in the same due to the formation of protective FeS film on the carbon steel surface. The mechanisms behind the corrosion and protection by different iron sulfide films have been discussed by Lee, Lewandowski, Morrison, et al. The iron sulfide film formed at low H2S concentrations, mainly composed of pyrite and troilite, was relatively protective. However, the iron sulfide film formed at high H2S concentration, mainly composed of mackinawite, was not protective. Thus, at low H2S concentration, the nature of the protective film is a dominant factor in the mechanism of the overall reaction. Consequently, the corrosion reaction is diffusion controlled. At high H2S concentration, the surface films become less protective and the corrosion becomes reaction controlled (Lee et al., 1993b). The composition and protectiveness of iron sulfide film depends upon the pH of the system. The least protective (mackinawite) film is formed when the pH of the medium is between 6.5 and 8.8. Outside this range, protective films of pyrrhotite and/or pyrite are formed. The carbon steel corroded very rapidly (1000 mpy) on initial contact with H2S and water, but subsequently, the iron sulfide corrosion products formed a protective film on the steel, which reduced the corrosion rate to <1 mpy. The corrosion resistance imparted by certain sulfide films, pyrite and pyrrhotite in particular, on carbon steel surfaces is clearly of major significance (Lee et al., 1993b).
The corrosion attack in anoxic hydrogen sulfide bulk liquid is not only by dissolved sulfides (DS) but also by precipitated iron sulfides. The nature of the various iron sulfides and their influence on the corrosion of steel have been reviewed by Smith and Miller (1975). The corrosiveness of the iron sulfides is based on their good electron conductivity, low overvoltage for hydrogen evolution, noble electrode potential, and defect structure. These properties cause iron sulfides to be excellent cathodes in galvanic corrosion cell with unreacted iron. Pyrrhotite, mackinawite, and greigite caused similar degrees of depolarization of iron, and pyrite was found to be the least active depolarizer (Smith & Miller, 1975).
In a recent series of experiments, the effects of suspended ferrous sulfide on the corrosion of mild steel were studied in an anaerobic biofilm reactor by Lee and Characklis (1993). The biofilm was developed on steel coupons in iron-free medium, followed by an increase in ferrous ion in the influent. Precipitation of ferrous sulfide (Fe2++HS-→ FeS+H+) took place mainly in the liquid phase. DS concentration in the effluent decreased as the ferrous ion concentration increased. Although iron sulfide particles accumulated in the biofilm, a low level of corrosion could only be observed. Addition of an iron-rich medium resulted in the precipitation of the entire biogenic sulfide, and nothing escaped in the effluent. Once the iron sulfide in the biofilm contacted the steel surface, the corrosion rate increased subsequently.
Introduction of oxygen into sulfide-bearing bulk liquid can also promote the formation of pyrite (Luther, 1991; Schoonen & Barnes, 1991). Luther (1991) demonstrated that pyrite can be formed very fast in the presence of polysulfide ions, ferrous iron, and DS at room temperature.
It should be emphasized that sulfide-covered surfaces can catalyze chemical transformations of sulfur compounds (Gragnolino & Tuovinen, 1984). For example, the reaction between ferrous sulfide and DO produces mainly elemental sulfur at neutral pH.
DS can also react with oxidized iron and form ferrous sulfide and elemental sulfur (Schmitt, 1991), as given in Equation (11).
Many literatures correlated the availability of ferrous ion with the corrosion by sulfide formation. Marchal, Chaussepied, and Warzywoda (2001) studied the effect of ferrous ion availability on SRB growth. They emphasized the crucial role of Fe2+ availability on the physiological properties of SRB and its relevance in the process of anaerobic biocorrosion. They proposed the biocorrosion mechanism in which the excretion of acidic products can promote Fe2+ availability for SRB. Lowering the pH by the metabolic products, such as acetic acid, increases the level of corrosive sulfides (H2S; HS-), which in turn promotes the attack of metallic iron, which produces Fe2+. The acidic conditions ensure Fe2+ for SRB growth and can account for the persistence of corrosion. Once SRB activity is established within the biofilm, iron sulfide nuclei quickly form and cover the steel surface as a result of the availability of sufficient ferrous and sulfide ions. At low ferrous ion concentrations, where an excess of sulfide ions results from bacterial growth, adherent and temporarily protective films of iron sulfides are formed on the steel surface, with a consequent reduction in the observed corrosion (Marchal et al., 2001). High corrosion rates by SRB are maintained only in the media containing high concentrations of ferrous ion. Consequently, the corrosion rate of mild steel is not controlled directly by SRB activity, but indirectly through the nature of reduced iron sulfides formed as corrosion products. The acceleration process is controlled by the cathodic reaction. Sun et al. (2011) investigated the interaction between SRB biofilm and carbon steel Q235 in soil extract solution (SES). They noticed a lower corrosion rate in SES with SRB during exponential growth period than during its decline period. The formation of iron oxide and some phosphorus compounds such as phosphide and hexaphosphate were noticed in SES. These compounds protect SRB from harmful substances like oxygen. The high corrosion during their growth decline period may be due to the removal of existing corrosion products with metabolic products.
The corrosive effect of sulfide and corrosion inhibitory effect of bacterial EPS produced by SRB on Q235 carbon steel were investigated (Bao, Zhang, Lv, & Wang, 2012). Bao et al. (2012) investigated the effect of two main metabolites of SRB on the corrosion of Q235 steels in 3.5% sodium chloride medium. They noticed that the presence of sulfide and EPS increases the anodic current density by nearly one order of magnitude. Subsequently, the feeble protective effect of EPS was also noticed in the presence of SRB. It can be concluded that the results supported the anodic depolarization mechanism in presence of EPS and H2S (anodic depolarization).
Enning et al. (2012) hypothesized a mechanism called electrical microbial influenced corrosion (EMIC) in which the direct, lithotrophic mode of iron utilization by direct electron uptake causes anaerobic corrosion by SRB, as given in Equation (12).
Enning et al. further explained the EMIC mechanism through the semiconductive sulfides, which are involved in the electron flow from the metal to the sulfate-reducing cells, which in turn increase the corrosion rates. The electron flow from the environment to the cell requires some electroconductive structures such as outer membrane and periplasmic membrane proteins. The above electron flow mechanism to the cells was earlier reported in bioleaching of metals and microbial fuel cells (Auernik, Maezato, Blum, & Kelly, 2008; Butler, Young, & Lovley, 2010). Yu, Duan, Du, Huang, and Hou (2013) also studied the accelerated anaerobic corrosion of electroactive SRB by electrochemical impedance spectroscopy and chronoamperometry using Postgate medium C. They suggested that SRB biofilm obtained electrons from carbon steel electrode polarized at -0.74 V. They also believed that the direct electron transfer occurs between SRB biofilm and carbon steel corrosion. The results also indicated that the electron transfer process did not require any soluble electroactive element mediator and that SRB biofilm likely played a key role in the electron transfer process. Yu et al. (2013) also substantiated the corrosion mechanism theory in which corrosion rate is accelerated by the electron flow. They observed a decrease in Ecorr of Q235 carbon steel immersed in SRB culture, which consumed electrons accumulated on the steel surface covered with rust or SRB metabolic products. Yu et al. (2013) claimed that stable cathodic H+ depolarization (Fe2+) causes electrons to accumulate on the steel surface and S2- formed by SRB metabolism accelerated the anodic reaction. Xu and Gu (2014) suggested that bioenergetic Fe0 oxidation releases more energy than lactate oxidation, but Fe0 cannot provide organic carbons needed for growth. They found that 90% and 99% carbon reductions increased the weight loss significantly. The experimental data also showed that 90% carbon reduction caused a 10-μm maximum pit depth, the largest among all other cases. The role of Fe as electron acceptor, elemental sulfur production, sulfides, and cathodic H2 in SRB corrosion of steels has been reviewed (Rabus et al., 2015). Zhang, Xu, Li, Yang, and Gu (2015) explained about electron mediators on the role of SRB. They suggested that iron oxidation happens outside the cells while the utilization of electron released by the oxidation process for sulfate reduction occurs in the SRB cytoplasm. They hypothesized that electron transfer is one of the bottlenecks in MIC by SRB.
Within the biofilm, the EPS produced plays an important role in the initial surface conditioning and transport of nutrients during and after biofilm formation. Uronic acid was detected in the EPS secreted by mesophilic SRB Desulfovibrio strain (Beech, Zinkevich, Tapper & Gubner, 1998). Accelerated corrosion of mild steel due to increased production of EPS in the presence of Cr3+ was observed (Fang, Xu, & Chan, 2000). The role of EPS in corrosion and corrosion inhibitory effects on carbon steel corroding thermophilic SRB was investigated by Dong, Liu, and Liu (2011). Although corrosion was inhibited by low amounts of EPS that forms a barrier on metal surface, which decreased oxygen reduction at 30°C, corrosion was enhanced with the increased levels of EPS. The increased anodic dissolution of the metal was observed due to the chelation of Fe ions by the EPS that accumulated on the metal surface (Dong et al., 2011). Venzlaff et al. (2013) studied the accelerated cathodic reaction in microbial corrosion of iron due to the direct electron uptake by SRB. They suggested that the attached cells reduced sulfate with electron derived from iron via conductive iron sulfide and the redox-active, cell-associated protein. Here, iron sulfide acts as a semiconductor and plays a significant role in anaerobic corrosion by mediating electron flow from the metal to cells. They concluded that hydrogen consumption by bacteria is not a decisive factor in MIC. Enning et al. (2012) found the corrosion effect of iron sulfide to be negligible in compact crusts formed by marine lithotrophic SRB and also suggested that further studies on the exact mechanism and contribution of iron sulfide to anaerobic corrosion are needed. Moreover, the Fe concentration thresholds for activating and switching off hydrogenase enzyme activity are SRB species-specific (Beech & Sunner, 2007). As bacterial uptake of cathodically generated H2, and thus the rate of the anodic reaction, is governed by the activity of hydrogenase, the rate of corrosion is expected to vary both with the ecology of SRB species within biofilm and with the local concentration of Fe2+ ions.
The present investigators understand that most of the SRB get electron from the organic molecules and some of the SRB get electron from the iron, and the involvement of extracellular enzymes viz. sulfide reductase and hydrogenase enzyme on sulfide reduction and hydrogen consumption, respectively, determines the electrochemical reaction of SRB on the metal system. The electron donors, viz. organic molecules, iron, and electron acceptors like sulfide, determine the electrochemical behavior. Few iron sulfides can contribute to additional cathodes, thus creating a galvanic cell, which enhances the corrosion of iron. It can be claimed that bacterial physiology is an important factor here for determining anodic/cathodic depolarization process.
2.4 Thermophilic SRB and its corrosion characteristics
2.4.1 Habitats of thermophilic SRB
SRB represent an important microbial group among the bacterial community in oil fields, refineries, and marine process industries that thrive over a wide range of salinities and temperatures and are perhaps ubiquitous to the ecosystem. Interestingly, H2, CO2, acetate, propionate, butyrate, and other short-chain organic acids, from C5 to C7, are often found in oil field waters, with acetate concentration being the highest. Molecular hydrogen is also found and can be produced from either geothermal reactions or thermophilic microbial fermentations. Many of the thermophilic SRB are known to perform dissimilatory sulfate reduction in the presence of acetate and/or butyrate. The habitats and characteristics of different thermophilic SRB have been presented in Table 1.
Characteristics and habitats of thermophilic SRB.
| S. no. | SRB species | Characteristics | Habitat | References |
|---|---|---|---|---|
| 1. | Desulfotomaculum species | Thermophilic and barotolerant | Oil field environments; Italian rice paddy soils | Rosnes, Torsvik, and Lien, 1991; Christensen, Torsvik, & Lien, 1992; Nilsen, Beeder, Thorstenson, & Torsvik, 1996 |
| 2. | Desulfotomaculum kuznetsovii | Gram positive, thermophilic, spore forming | Underground thermal mineral water ecosystem; refinery cooling towers | Nazina, Ivanov, Kanchaveli, & Rozanova, 1988; Anandkumar et al., 2009a |
| 3. | Desulfotomaculum thermocisternum | Growing at 62°C, oxidizing lactate, ethanol, butanol, carboxylic acids | Norwegian sector of North Sea | Nilsen, Torsvik, & Lien, 1996 |
| 4. | Desulfacinum infernum | Thermophilic (60 C), Gram negative, complete oxidizer of acetate, butyrate, palmitate, and alcohols | Gullfaks oil field in the North Sea | Rees, Grassia, Sheehy, Dwivedi, & Patel, 1995 |
| 5. | Thermodesulforhabdus norvegicus | Thermophilic Gram-positive, oxidizes acetate, butyrate, and palmitate | Gullfaks oil field in the North Sea | Beeder, Torsvik, & Lien, 1995 |
| 6. | Thermodesulfobacterium mobile (formerly known as Desulfovibrio thermophilus) | Thermophilic (80°C) Gram positive | North Sea oil reservoir | Rozanova & Pivovarova, 1988; Christensen et al., 1992 |
| 7. | Thermodesulfobacterium commune | Thermophilic (80°C), Gram positive | Continental oil reservoir located in the East Paris Basin | L’Haridon, Reysenbacht, Glénat, Prieur, & Jeanthon, 1995 |
| 8 |
Desulfovibrio cavernae
Desulfotomaculum geothermicum |
Thermophilic (50°C) | Deep subsurface sandstones (Berlin); oil refinery cooling towers | Sass & Cypionka, 2004; Anandkumar et al., 2009b |
| 9. | Archaeoglobus fulgidus | Hyperthermophilic archaea | Hot oil field waters of the North Sea (Norway) | Beeder, Nilsen, Rosnes, Torsvik, & Lien, 1994 |
| 10. | Desulfovirgula thermocuniculi | Thermophilic (60°C– 80°C) | Geothermal underground mine in Japan | Kaksonen, Spring, Schumann, Kroppenstedt, & Puhakka, 2007 |
| 11. | Desulfotomaculum solfataricum | Thermophilic (60°C) | Hot solfataric fields in northeast Iceland | Goorissen, Boschker, Stams, & Hansen, 2003 |
| 12. | Desulfosoma caldarium | Thermophilic (50°C–62°C) | Hot spring located at a height of 2500 m in the Colombian Andes, Colombia | Baena, Perdomo, Carvajal, Dıaz, & Patel, 2011 |
| 13. | Archaeoglobus sp., Desulfacinum sp. Desulfotomaculum sp. | Thermophilic (60°C) | Two high-temperature oil production systems of Dan and Halfdan, Denmark | Gittel, Sørensen, Skovhus, Ingvorsen, & Schramm, 2009 |
2.4.2 Corrosion by thermophilic SRB
Considerable works had been centered only on the role of mesophilic SRB Desulfovibrio species in the corrosion process. Very few works were published on corrosion by thermophilic SRB; corrosion influenced by SRB species belonging to the genus Desulfotomaculum is only sparingly discussed (Almeida & de Franca, 1999; Ren & Wood, 2004; Villanueva et al., 2006; Duncan et al., 2009; Anandkumar et al., 2009a; Anandkumar et al., 2009b). Thermophilic SRB metabolism leads to accumulation of an organic complex on the steel surface that suppresses the anodic reaction, for example, by lactate metabolizer D. geothermicum (Anandkumar et al., 2009b) and acetate metabolizer D. kuznetsovii (Anandkumar et al., 2009a). Schick (1999) observed that the elevated temperatures are known to encourage SRB growth. Corrosion of nickel and titanium alloys by thermophilic SRB was reported by Little, Wagner, Gerchakov, Walch, and Mitchell (1986) and Little, Wagner, and Ray (1993a), respectively. Little et al. (1986) observed the thermophilic corrosion of nickel 201 “T” brazed joints maintained at 60°C by thermophilic bacteria. Thermophilic microorganisms resemble their mesophilic counterparts in terms of growth requirements and tolerance. The nickel braze joint failure at 60°C was mainly due to anodic corrosion current because of the differential aeration cells and acidic metabolites formed by bacteria. At high temperature, activation energy barriers were overcame, and the acids were effective in accelerating corrosion. Potential differences with subsequent enhanced currents could be observed due to oxygen-deficient and even oxygen-free conditions formed beneath biofilms as oxygen is taken up by respiring microorganisms as rapidly as it diffuses to the surface. Corrosion current is zero when oxygen gas is bubbled through both cells of the experimental apparatus at 23°C. However, at 60°C, the electrode in the compartment depleted of oxygen became the anode with an increase in current. Acidic metabolites secreted by microorganisms can prevent passivation or destroy an existing passive film. Nickel forms a passivating film in slightly alkaline solutions. Most heterotrophic bacteria secrete organic acids during the fermentation of organic substrates. The types and amounts of acids produced in nature depend on the kinds of organisms present and the substrate molecules available. Organic acids from a wide range of bacteria have been shown to enhance the corrosion of a number of different types of metal. Acids were evaluated abiotically for their contribution to the overall corrosion current at room temperature and 60°C. However, at 60°C, the electrodes exposed to isobutyric and isovaleric acids became the anodes and the corrosion current increased. It is recognized that at the site of acid production, under the biofilm at the metal/biofilm interface, the concentrations of acidic metabolites are much greater, and their impact is amplified (Little et al., 1986). SRB corrosion studies with titanium and stainless steel by Little, et al. (1993a) showed increase in Ecorr continuously for the stainless steel, but not for titanium because of the poor catalytic activity of the titanium oxide layer, which does not allow increase in the rate of oxygen reduction with time. The resistance of metals to corrosion is strongly influenced by temperature. The minimum temperature for crevice corrosion in titanium alloys is 75°C. Titanium alloys are fully resistant to bacterially synthesized hydrogen adsorption at 100°C and also resistant to reduced chemical species (ammonia, sulfides, hydrogen sulfide, nitrites, ferrous ions, and organosulfur compounds) resulting from anaerobic microbial activity at temperatures up to 100°C. Under anaerobic reducing conditions, titanium oxide films remain intact down to pH±2 at 100°C. Titanium had low corrosion rates under the exposure conditions, with no localized attack and no hydride formation when exposed to a thermophilic hydrogen-producing bacterium. However, uniform corrosion and pits could be observed on titanium with 12-week-old mixed biofilm formed by mesophilic SRB Desulfovibrio ferrophilus and manganese oxidizing bacterium Bacillus flexus at 37°C (Anandkumar, Nanda Gopala Krishna, George, Parvathavarthini, & Kamachi Mudali, 2013).
Pitting of stainless steel 304 (SS304) by SRB Desulfotomaculum nigrificans at 50°C has been reported by Torres-Sanchez, Garcia-Vargas, Alfonso-Alonso, and Martinez-Gomez (2001). They compared the corrosion characteristics of two thermophilic bacterial cultures (D. nigrificans growing at 50°C – strain A and Bacillus sp. growing at 90°C – strain B). The presence of thermophilic bacteria displaced the corrosion potential toward the negative direction. In the system inoculated with strain B (90°C), there was a quick fall in corrosion potential. The passive loop of the active-passive regions is not revealed, and the passive current density (ipass) remained at a very low value. Once passivity has been lost, the anodic polarization curve showed dramatic increase in the anodic current, and consequently, pitting attack initiated. The presence of both strains in growth media caused the displacement of corrosion potentials toward more negative values. Thus, the growth media inoculated with this thermophilic SRB became more negative in a more active environment (Torres-Sanchez et al., 2001). The corrosion potential displacement is faster in the presence of strain A, and corrosion is also much more aggressive than strain B. This aggressivity is manifested by the displacement of corrosion potential toward negative values and the lowest value of pitting potential in the system inoculated with strain A.
The complete oxidation of lactate and the presence of acetyl-CoA oxidation pathway are usually associated with the ability to use free lactate as a growth substrate. Widdel (1988) also assessed lactate as an organic substrate for enrichment of sulfate reducers and described sulfate reduction using lactate as an electron donor as described in Equation (13) (ΔG=-34.2 kJ/mol; Peck & LeGall, 1982).
SRB shifts the potential to negative because iron sulfide acts as cathodic to the parent metal. The formation of iron sulfide is also not uniform due to the heterogeneity of the biofilm, and this may create an electrochemical cell on the metal surface, enhancing corrosion at high temperature. The precipitated ferrous ions with the sulfide ions as iron sulfide act as an additional cathode, which can enhance corrosion. Mesophilic SRB D. propionicus enhanced anodic and cathodic currents by the formation of iron sulfide, which formed an additional cathode to the parent metal (Anandkumar et al., 2010). The total exchange current for hydrogen reduction is the product of the exchange current density and the effective cathodic area. If it is assumed that hydrogen ion discharge and electron transfer are occurring on and through the accumulated sulfides, it would be expected that an increase in the effective surface area of sulfide would lead to an increase in the cathodic reaction rate.
Oxide films formed on steel surfaces exposed to aerobic environments provide protection against further corrosion. SRB growth reduces the stability of the protective film and enhances corrosion processes. The enhanced corrosion rate due to the SRB activity in aerobic systems occurs through the anodic and cathodic depolarization with the transformation of iron oxide to iron sulfides. Eventually, cathodic depolarization controls the corrosion process. The mechanistic differences between SRB-enhanced corrosion of mild steel in a totally anaerobic system and in an aerobic system lie in the nature of the corrosion products. Only the reduced iron sulfides (such as mackinawite and greigite) are detected in a totally anaerobic system (McNeil & Little, 1990), and they are not permanently cathodic toward mild steel (Craig, 1991). The activity of SRB is required in this system to maintain the electrochemical activity of ferrous sulfide. However, in an aerobic system, the oxidized iron sulfides (such as pyrite) and elemental sulfur were detected in addition to the reduced iron sulfides (Lee et al., 1995). The mild steel corrosion by pyrite is not well understood when compared with the more reduced iron sulfides and the mild steel corrosion by elemental sulfur is clearly illustrated as shown in Equation (14) (Tiller, 1985).
Once the environmental conditions for the elemental sulfur corrosion mechanism are established, the corrosion process is autocatalytic. Consequently, continuing SRB activity may not be required to maintain the corrosion process (Tiller, 1985).
2.4.3 Influence of temperature and pressure on electrochemical behavior of SRB
Equipment failures can have serious consequences because processes at high temperatures usually involve high pressures as well. The possibility for living organisms to survive or thrive in oil field environments depends on the physical characteristics and chemical composition of the ecosystem (Stetter, Hoffmann, & Huber, 1993a). Temperature is the main limiting factor for microbial growth in oil reservoirs. As temperature increases with depth at a mean rate of 3°C per 100 m (but regional geothermal gradients may be significantly different), deep oil reservoirs, which attain an in situ temperature exceeding 130°C–150°C, cannot sustain bacterial growth. This temperature range is considered the highest theoretical limit for growth due to the thermal instability of biological molecules (Stetter et al., 1993a). Different types of data suggest that the presence of indigenous bacteria in oil fields could be limited to a threshold temperature range of 80°C to 90°C. Hyperthermophilic microorganisms growing at temperatures as high as 103°C have been isolated from some reservoirs, and the authors suggested that they represented exogenous bacteria resulting from seawater injections (Stetter et al., 1993b; Grassia, McLean, Glénat, Bauld, & Sheehy, 1996). Magot, Hurtevent, and Crolet (1993) described the localized growth of SRB in well tubings, resulting in the so-called well souring phenomenon. Because of their detrimental effects, SRB have been the most commonly studied bacterial group from oil field waters. A distinction is generally made between mesophilic SRB, which are merely involved in corrosion processes of top facilities, and thermophilic SRB, mainly responsible for in situ reservoir souring. Liu, Liu, Hu, Zhou, and Zheng (2009) explained the influence of temperature on corrosion by SRB. Fe2+ ions consume the corrosive sulfides produced by thermophilic SRB and the iron sulfides adsorbed on the steel surface. The biofilm getting thickened with the bacterial metabolism and metabolites of active bacteria in the biofilm accelerated pitting corrosion at 60°C due to the possible transmission of the electrons and electrolyte between the biofilm and the environment. SRB corrosion rates of nickel were high at high temperature (~80°C) when oxygen diffusion to the metal surface creates the oxygen concentration cells on the metal surface. Corrosion process was enhanced due to very high potential differences in the oxygen differentiation cells (Little et al., 1993b). Generally, at higher temperature, the corrosion rate increases. However, reduced corrosion rates are also observed at high temperatures due to the increase in precipitation with temperature, leading to protective film formation. The influence of temperature on protective film formation is quite complex. The complexity is due to the nature of the different protective films. Again, the increase in temperature alleviate desorption of physically adsorbed protective film and thereby increases corrosion rate of the metal The strength of the chemisorbed layers increases when temperature increases and the protection lasts until the complete degradation of layer occurred. Another aspect to be considered at high temperatures is the increased diffusion of chloride ions leading to pitting by thermophilic SRB (Anandkumar et al., 2009a; Anandkumar et al., 2009b).
Stott and Herbert (1986) studied the effects of elevated pressures and temperatures on the growth, morphology, and metabolic activity of SRB isolated from the North Sea. Pressure, temperature profiles, growth curves, and sulfate reduction rates are presented for several isolates. The maximum pressure and temperature that supported growth were 65,000 kPa and 45°C, respectively. At the above temperatures and pressure, sulfate reduction accompanied the growth and resulted in production of sulfides (Stott & Herbert, 1986). Rosnes, et al. (1991) identified two strains of thermophilic SRB from the different oil fields in the North Sea, and the strain analyses showed similarities in most characteristics of the genus Desulfotomaculum. The identified strain T93B produced H2S at 78°C and 300-bar (30-MPa) conditions, which resemble oil reservoir environments. Lappin-Scott, Bass, McAlpine, and Sanders (1994) observed an indigenous population of thermophilic SRB in water injection and oil production areas of three facilities in the North Sea. During nutrient starvation and extreme conditions, thermophilic SRB cells could attach to production equipment and form a corrosive biofilm. They are also able to survive when discharged overboard in separated production waters and have the potential to adhere to any structural production equipment in open sea situations. When the environmental conditions become favorable, biofilms containing thermophilic SRB on such structures have the potential to cause corrosion. They have also shown that starved thermophilic SRB are able to survive very long periods in cold aerobic seawater, which suggests that the risk of corrosion initiation is high on marine surfaces and in oil production facilities. This can result in the generation of sufficient hydrogen sulfide for corrosion problems to develop in the production facilities. The implication is that these bacteria are able to grow and generate hydrogen sulfide in situ, at the pressures and temperatures within the oil reservoir. The generation of hydrogen sulfide by SRB may lead to increased hydrogen sulfide levels (souring) in oil and gas and to corrosion problems in production facilities. The pitting corrosion rate is increased at high pressure, facilitating the dissolution of metal. The pitting corrosion rate is decreased if the pressure involves in the formation of intact surface layers. The bacteriostatic effects of a number of commercial biocides were enhanced at elevated hydrostatic pressures and temperatures (Stott & Herbert, 1986). They suggested that the concentration of an inhibitory substance required to control SRB in a high-pressure system is generally considerably less than the concentration of the same substance required at atmospheric pressure. Economy loss in process industries due to MIC involved by various groups of microbes especially by thermophilic SRB may be reduced to a large extent by extensive studies in understanding the influence of temperature and pressure in corrosion at extreme conditions.
3 Molecular biology in SRB studies
3.1 Taxonomy of SRB
A clear picture for SRB taxonomy has not been presented in the 1920s to the 1940s due to impure cultures and the use of inappropriate culture media. Dissimilatory sulfate reduction was selected as the primary taxonomic character among 116 biochemical characters to survey 92 SRB isolates and found only 26 subsidiary characters that were to be of taxonomic value (Skyring, Jones, & Goodchild, 1977). Classification with fatty acid methyl esters by gas chromatography values covers a wide range in many genera. Castro, Williams, and Ogram (2000) reviewed all works done for taxonomy of SRB and assembled the representative 16S rRNA sequences reported for SRB to place them under four groups. They constructed phylogenetic trees and divided SRB into four groups based on rRNA sequence analysis: Gram-negative mesophilic SRB, Gram-positive spore-forming SRB, thermophilic bacterial SRB, and thermophilic archaeal SRB.
Gram-negative mesophilic SRB is located within the delta subdivision of the Proteobacteria, and it comprises two families, namely Desulfovibrionaceae and Desulfobacteriaceae. The genera Desulfovibrio and Desulfomicrobium are included in the Desulfovibrionaceae family. The Desulfobacteriaceae family included all SRB within the δ-Proteobacteria that were not part of the Desulfovibrionaceae (Devereux et al., 1990; Widdel & Bak, 1992). This rather broad definition included species of the genera Desulfobulbus, Desulfobacter, Desulfobacterium, Desulfococcus, Desulfosarcina, Desulfomonile, Desulfonema, Desulfobotulus, and Desulfoarculus (Devereux et al., 1990; Widdel & Bak, 1992).
A single family of SRB has been proposed within the Gram-positive SRB, and the genus Desulfotomaculum is placed within low-Guanine-CytosineQ5 (GC) Gram-positive bacteria such as Bacillus and Clostridium (Castro et al., 2000). Members of the genus Desulfotomaculum form heat-resistant endospores, a characteristic identical with many Bacillus and Clostridium species. In contrast with the mesophilic SRB, some species of Desulfotomaculum are thermophilic, although their optimal growth temperatures are lower than those of thermophilic Gram-negative and archaeal sulfate reducers. Although most spore-forming SRB are found in similar environments to δ-Proteobacteria SRB, spore formation allows this group to survive for long periods of desiccation and oxic conditions. Mori, Kim, Kakegawa, and Hanada (2003) updated SRB taxonomy with a fifth lineage, the Thermodesulfobiaceae.
The two well-characterized thermophilic bacterial SRB, Thermodesulfobacterium commune (Zeikus, Dawson, Thompson, Ingvorsen, and Hatchikian, 1983) and Thermodesulfovibrio yellowstonii, were isolated from hydrothermal vent waters in Yellowstone National Park (Henry et al., 1994), and their optimal growth temperatures are higher than those described for Gram-positive spore-forming thermophilic SRB, but lower than those of the archaeal SRB. Although these two genera have similar physiological and phenotypic characteristics, they differ in shape and GC content for T. yellowstonii and T. commune, respectively. Henry et al. (1994) suggested that categorization of thermophilic SRB (similar physiology but different phylogeny) is similar to the situation with the Desulfovibrio family: a group that shares physiological similarities but is phylogenetically diverse and is grouped within a family. Moreover, both thermophilic SRB and Desulfovibrio sp. exhibit incomplete oxidation of acetate and utilize a limited number of electron donors. Archaeal thermophilic SRB exhibits optimal growth temperatures above 80°C. Two species have been well described under archaeal thermophilic SRB to date: Archaeoglobus fulgidus and Archaeoglobus profundus were isolated and identified from marine hydrothermal systems by Stetter (1988) and Burggraf, Jannasch, Nicolaus, and Stetter (1990), respectively. Flagellated A. fulgidus are facultative chemolithoautotrophs producing small amounts of methane, whereas obligate chemolithoheterotrophs A. profundus do not possess flagella or produce methane (Burggraf et al., 1990).
3.2 Molecular methods adopted in SRB taxonomic studies
Biotechnology has played an important role in understanding the taxonomy and physiology of SRB in many aspects. Different techniques of molecular biology adopted in SRB taxonomic studies with references have been presented in Table 2. Identification of SRB with culture-dependent and culture-independent methods at adverse conditions are being done using molecular techniques such as 16S rRNA sequence analysis, polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis (DGGE), quantitative PCR (qPCR), fluorescence in situ hybridization (FISH) method, confocal laser scanning microscopy (CLSM), two-dimensional gel electrophoresis, functional gene markers (dsrAB and apsA) analysis, microarray, etc. Besides these molecular techniques, metagenome sequencing plays a predominant role in analyzing microbial populations of extreme conditions such as acid mines and sulfur deposits where microbial cultivation techniques cannot give a complete profile. Cost-effective metagenome sequencing supersedes the conventional sequencing procedures and helps in whole genome sequencing of many microbes and whole biofilms growing in extreme habitats. Multiphasic approaches by combining all the above methods to identify and quantify SRB in environments are being currently practiced. In addition to these techniques, recombinant DNA technology is also paving ways for studying the recombinant enzymes expressed from genes of SRB in structural and functional aspects discussed in the later sections.
Biotechnology methods adopted in SRB studies.
| S. no. | SRB species | Techniques employed | Applications | References |
|---|---|---|---|---|
| 1. | Archaea and bacteria | 16S rRNA sequencing | Identification of SRB from different environments | Rabus, Fukui, Wilkers, & Widdel, 1996; Voordouw et al., 1996; Daly, Sharp, & McCarthy, 2000 |
| 2. | Many genera including Desulfobulbus, Desulfotomaculum, Desulfonema, Desulfosarcina, Desulfococcus | dsrAB, hyd, apsA, sequencing | As function gene markers to identify and confirm the SRB species from the different environments | Klein et al., 2001; Friedrich, 2002; Zverlov et al., 2005; Leloup, Quillet, Berthe, & Petit, 2006; Miletto, Bodelier, & Laanbroek, 2007; Anandkumar, 2009 |
| 3. | Major phylogenetic groups of SRB | FISH probes | Spatial distribution | Hristova et al., 2000; Lücker et al., 2007 |
| 4. | Desulfovibrio sp. Desulfomicrobium sp. Desulfotomaculum sp. | 16S rRNA phylochip | SRB from acidic fen soils | Loy et al., 2002 |
| 5. | Archaeoglobus sp. Desulfovibrio sp. Desulfotomaculum sp. Desulfobulbus sp. | dsrAB phylochip | Microarray and functional gene analysis of SRB in low-sulfate acidic fen soils | Loy, Kusel, Lehner, Drake, & Wagner, 2004 |
| 6. | Desulfotalea sp. Desulfofustis sp. | Amplified ribosomal DNA restriction analysis, terminal restriction fragment length polymorphism (TRFLP) | Identification of psychrophilic SRBs in Arctic Ocean | Ravenschlag, Sahm, Pernthaler, & Amann, 1999 |
| 7. | Desulfotomaculum sp. Desulforhabdus sp. Desulfobacterium sp. Synthrophobacter sp. | Qpcr | Quantification of SRB present in rice field soils, soda lakes, industrial waste waters | Stubner, 2002; Stubner, 2004 |
| 8. | Desulfobacterium catecholicum, Desulfocapsa sp. Desulfosarcina sp. | Catalyzed reporter deposition (CARD)-FISH | Vertical distribution of SRB in intertidal mud-flat samples | Mussmann, Ishii, Rabus, & Amann, 2005 |
| 9. | Desulfotomaculum acetoxidans, Desulfobacter sp. | Stable isotope probing (SIP) | Determination of SRB population with composition of phospholipids fatty acids | Boschker et al., 1998; Webster et al., 2006 |
| 10. | Desulfobulbus sp., Desulfovibrio sp. | Microautoradiography (MAR)-FISH | Relative abundance of SRB in sewer biofilms and their substrate uptake patterns | Ito, Nielsen, Okabe, Watanabe, & Nielsen, 2002 |
| 11. | Desulfovibrio alaskensis | CLSM and two-dimensional gel electrophoresis | Biofilm formation and proteomics of biofilms | Wikiel et al., 2014 |
| 12. | Desulfotomaculum, Desulfonema, Desulfosarcina, Desulfococcus, Desulfovibrio, Desulfomicrobium | DGGE | SRB diversity with variable regions of 16S rRNA gene | Neria-Gonzalez, Wang, Ramırez, Romero, & Hernandez-Rodrıguez, 2006; Balamurugan, Joshi, & Rao, 2011 |
| 13. | Desulfobacteraceae, Desulfobulbaceae, Desulfoarculaceae, Desulfovibrionaceae, Desulfonatronumaceae | qPCR and DGGE | SRB diversity of marine steel structures | Païssé et al., 2013 |
| 14. | Dulfovibrio piger | Transposon mutagenesis (insertion sequencing); multiplex pyrosequencing | SRB identification with α-subunit of adenosine 5′-phosphosulfate reductase in human gut | Rey et al., 2013 |
| 15. | Sulfate producing Deltaproteobacterial group | Protein-based SIP (protein-SIP) | Metaproteome analysis of benzene degrading SRB communities using high resolution mass spectrometry for the detection and quantification of mass shift related with heavy isotope labels in proteins | Taubert et al., 2012 |
| 16. | Desulfobulbus group | Multicolor CARD-FISH | Consortia of SRB with methanotrophic archaea | Schreiber, Holler, Knitte, Meyerdierks, & Amann, 2010 |
| 17. |
Desulfovibrio group Desulfococcus group Pyrobaculum sp., Caldivirga sp. |
Metagenome sequencing multiple-pathway and protein-specific functional genes | SRB identification in extremely acidic mine-drainage biofilms of Joseph’s Coat Springs, Calcite Sites of Yellowstone National Park | Inskeep et al., 2010 |
3.3 Molecular biology studies adopted in SRB physiology
3.3.1 Metabolic gene analysis in completed SRB genomes
Whole genomes of 3 archaeal SRB and 16 bacterial SRB have been completely sequenced, as given in Tables 3 and 1 more SRB genomes are being sequenced (www.microbesonline.org). Forty-one orthologous genes are present in the above 19 sequenced genomes. Based on the whole genome sequence information of 19 SRBs (www.microbesonline.org), sulfate metabolism and tricarboxylic acid (TCA) cycle metabolism have been analyzed for the above 19 genomes listed in Table 3 with references. Figures 1 and 2 describe the differences in the above two metabolic pathways of sequenced 19 SRB genomes. Analysis of archaeal SRB genomes shows the absence of some of the intermediate reactions in the sulfate reduction and TCA cycle. The oxidation of organic substrates by SRB may either be complete forming CO2 or incomplete with acetate usually as the end product. The acetyl-CoA oxidation pathway is absent in incomplete oxidizers such as Desulfovibrio sp. and Thermodesulfobacterium sp. (Widdel, 1988). The presence of a pathway for acetyl-CoA oxidation is usually associated with the ability to also use free acetate as a growth substrate. Desulfotalea psychrophila LSv54 and Desulfovibrio magneticus RS-1 having two plasmids each encode xenobiotics degrading genes. CO utilizer and N2 fixer Desulforudis audaxviator, a dominant deep subsurface SRB has been sequenced and revealed the ancient mode of metabolism that might sustain life on other planets (Chivian et al., 2006). Larger, genome-sized (5.6-Mb) chemolithoautotroph Desulfobacterium autotrophicum HRM2 has been sequenced, and the Wood-Ljungdahl pathway for complete oxidation of acetyl CoA to CO2 has been analyzed (Strittmatter et al., 2009). The whole genome of A. fulgidus was sequenced, and genes responsible for different carbon metabolism were analyzed (Klenk et al., 1997). High levels of CO2, formate, and acetate formation were observed in the presence of sulfate in A. fulgidus, a thermophilic sulfate-reducing archaeon (Henstra, Dijkema, & Stams, 2007). Pereira et al. (2011) discussed the energy metabolism of sulfate-reducing organisms and analyzed the chemiosmotic and flavin-based electron bifurcating mechanisms from the sequenced genomes of SRB. Pereira et al. (2011) also reviewed the involvement of electron donors and enzymes such as cytoplasmic [NiFe] and [FeFe] hydrogenases, formate dehydrogenases, and heterodisulfide reductase-related proteins in energy metabolism.
Information about genome sequenced SRBs analyzed in this study used for metabolic pathway analysis (Figures 1 and 2).
| S. no. | Species with phylum | Abbreviations used in figures | Genome size (Mb) | Remarks |
|---|---|---|---|---|
| 1 | Euryarchaeota Archaeoglobus fulgidus DSM4304 |
Af | 2.1 | Klenk et al., 1997 |
| 2 | Archaeoglobus profundus DSM5631 | Ap | 1.5 | 2.8-kb plasmid |
| 3 | Crenarchaeota Caldivirga maquilingensis IC-167 |
Cm | 2.0 | |
| 4 | Proteobacteria Desulfobacterium autotropicum HRM2 |
Dba | 5.5 | 68-kb plasmid Strittmatter et al., 2009 |
| 5 | Desulfohalobium retbaense DSM 5692 | Dhr | 2.8 | 45-kb plasmid |
| 6 | Desulfomicrobium baculatum DSM 4028 | Dmb | 3.9 | |
| 7 | Desulfotalea psychrophila LSv54 | Dtp | 3.5 | 121- and 14-kb plasmids Rabus et al., 2004 |
| 8 | D. desulfuricans G20 | Dvd | 3.7 | |
| 9 | D. desulfuricans subsp. desulfuricans ATCC27774 | Dvdsp | 2.8 | |
| 10 | Desulfovibrio magneticus RS-1 | Dvm | 5.2 | 8- and 58-kb plasmids |
| 11 | Desulfovibrio salexigens DSM 2638 | Dvs | 4.2 | |
| 12 | Desulfovibrio vulgaris Hildenborough | DvvH | 3.5 | 202-kb plasmid Heidelberg et al., 2004 |
| 13 | Desulfovibrio vulgaris DP4 | DvvD | 3.4 | 198-kb plasmid |
| 14 | Desulfovibrio vulgaris Miyazaki F | DvvM | 4.0 | |
| 15 | Syntrophobacter fumaroxidans MPOB | Sfu | 4.9 | |
| 16 | Firmicutes Desulforudis audaxviator MP104C |
Dra | 2.3 | |
| 17 | Desulfotomaculum acetoxidans DSM771 | Dta | 4.5 | |
| 18 | Desulfotomaculum reducens MI-1 | Dtr | 3.6 | |
| 19 | Nitrospirae Thermodesulfovibrio yellowstonii DSM11347 |
Tdy | 2.0 |
Sulfate metabolism in whole genome sequenced SRBs.
Citric acid metabolism in whole genome sequenced SRBs.
3.3.2 Structures and functional studies on hydrogenase (hyd) proteins
Hydrogen plays a central role in the energy metabolism of SRB of the genus Desulfovibrio, which can either utilize or produce hydrogen depending on growth conditions (Fauque et al., 1988; Rabus et al., 1996). Hydrogenases (hydrogen: oxidoreductase EC.1.12) constitute a class of enzymes that are highly diversified in their active center composition and structure. The involvement of hydrogenases, which are either present in bacteria or free in solution, remains subject to many debates. Bryant et al. (1991) have demonstrated that there is a direct correlation between the presence of hydrogenase in SRB and corrosion.
Desulfovibrio hydrogenases are subdivided into three groups, the [Fe] hydrogenases, the [NiFe] hydrogenases, and the [NiFeSe] hydrogenases. There are marked differences among the three types of enzymes with respect to their catalytic activities; their sensitivity to CO, NO, NO2-, and acetylene (He et al., 1989); and their molecular structures (Fauque et al., 1988). A significant degree of sequence homology was found between the genes of Desulfovibrio gigas (D. gigas) and a Desulfomicrobium baculatum-like strain coding for the large and small subunits of the [NiFe] and the [NiFeSe] hydrogenase, respectively (Voordouw et al., 1989a). In the case of the [Fe] hydrogenase, the hydA and hydB genes for the large and small subunits in Desulfovibrio vulgaris Hildenborough and D. vulgaris subsp. oxamicus are highly homologous (Voordouw, Strang, & Wilson, 1989b); however, there is no significant homology between the [Fe] hydrogenases and the [NiFe] hydrogenases. The oxidation of hydrogen by the periplasmic hydrogenases of Desulfovibrio strains is thought to generate a proton gradient (proton-motive force, pmf) through vectorial electron transfer; in this system, the protons from H2 are left in the periplasm and only the electrons are channeled through the membrane to the cytoplasmic electron acceptors (Badziong & Thauer, 1980).
The generation of a proton gradient by simple charge separation due to a periplasmic hydrogenase would leave eight extracellular protons per mole of sulfate being reduced. As one of these protons may enter the cell during sulfate transport (Cypionka, 1989), seven protons would be left for chemiosmotic energy conservation, yielding 0.66 mol ATP (Thauer & Morris, 1984) per mole of sulfate reduced with H2. As 2 mol ATPs are consumed for sulfate activation, 0.33 mol ATP would remain for cell synthesis. This is much lesser than the values estimated from growth yields that suggest a net synthesis of 1.3 mol of ATP per mole of sulfate (Nethe-Jaenchen & Thauer, 1984). Proton translocation with H2 and sulfate has been measured in D. desulfuricans strain Essex 6, a strain in which hydrogenase is cytoplasmic or at least on the cytoplasmic aspect of the membrane (Fitz & Cypionka, 1989). Strains of other Desulfovibrio sp. translocated protons with H2 and nitrite, even though hydrogenase and nitrite reductase were both periplasmic enzymes (Barton, LeGall, Odom, & Peck, 1983); this excludes generation of a proton gradient by simple vectorial electron flow via the membrane. Growth of the Gram-positive Desulfotomaculum orientis on H2 with high cell yields demonstrated that chemiosmotic ATP synthesis does not require a periplasmic hydrogenase (Cypionka & Pfennig, 1986).
3.3.3 Structures and functional studies on dissimilatory sulfite reductase (dsr) proteins
Sulfate is metabolized to sulfide through four steps catalyzed by enzymes such as ATP sulfurylase (SO42- to APS), APS reductase (APS to SO32-), and dissimilatory sulfite reductase (SO32- to S2-). ATP sulfurylase and dissimilatory sulfite reductases (dsr) are the functional gene markers in SRB identification. Sulfite reductases have been focused with respect to its structures and functions in SRB. dsr are classified according to their ultraviolet and visible absorption spectra: desulfofuscidin (LeGall & Fauque, 1988), desulforubidin (Lee et al., 1993a; Arendsen et al., 1993), and desulfoviridin (Lee et al., 1993b; Wolfe, Lui, & Cowan, 1994). dsr consist of relatively long polypeptide chains containing both semi-conserved and highly conserved regions and occur in sulfate- and sulfite-reducing prokaryotes as well as in some sulfur oxidizers (Karkhoff-Schweizer, Huber, & Voordouw, 1995; Hipp et al., 1997; Meyer & Kuever, 2007).
Comparative analysis of dsr structures: A total of 17 structures have been elucidated for dissimilatory sulfite reductase and deposited in the Protein Data Bank (PDB) (www.rcsb.org) by various researchers. Three structures having PDB IDs 2V4J, 3C7B, and 1SAU have been taken from PDB for dsr structural analysis. The structural comparisons of the dsr from the published data of dsr protein structures (Figure 3) of A. fulgidus (Schiffer et al., 2008) and D. vulgaris (Oliveira et al., 2008) reveal that the proteins belong to α-β class proteins. Archael and eubacterial proteins share >85% similarity in their structures. One to two chains and three to four chains of dimeric chains of dsr protein of pentameric A. fulgidus 3C7B (Schiffer et al., 2008) and hexameric D. vulgaris 2V4J (Oliveira et al., 2008), respectively, share structural similarity (Figure 4) among them, which might have occurred due to gene duplication. Five and six chains of 2V4J were with compared with the γ-subunit of DsrC of A. fulgidus 1SAU (Weiss et al., 2004.) The dsr structure of D. vulgaris analyzed by Oliveira et al. (2008) gives an idea about the link between eubacteria and archaeon. The protein structure has five-stranded β-sheet bundled with several α-helices where the [4Fe4S] cluster bound by DsrA is in close proximity to a sirohydrochlorin group (a demetallated siroheme), which gets buried in the interior of the protein and sits on the interface between DsrA and DsrB (Oliveira et al., 2008). The structure of the A. fulgidus (Schiffer et al., 2008) includes only the α2β2 unit of DsrAB and is quite similar to the structure of the DsrAB proteins from D. vulgaris, apart from some small differences in the N and C termini of both subunits and two longer loops in the ferredoxin domains. The most noteworthy difference is the fact that dsr from A. fulgidus has four sirohemes and no sirohydrochlorin localization of sulfite reductases in the membrane region. Structural similarity among the dimeric chains (1 and 2; 3 and 4) reveals that the proteins belong to α- and β-class proteins. Mander et al. (2005) determined the X-ray structure of the γ-subunit of the dissimilatory sulfite reductase (dsrC) from A. fulgidus in the two crystal forms named dsrCnat and dsrCox. Cort et al. (2001) determined the solution structure of γ-subunit dsrC of sulfite reductase in Pyrobaculum aerophilum (P. aerophilum) with NMR spectroscopy. The fold corresponds to that of the homologous protein from P. aerophilum but is significantly more compact. The most interesting, highly conserved C-terminal arm adopts a well-defined conformation in A. fulgidusdsrC in contrast to the completely disordered conformation in P. aerophilumdsrC. They discussed functional relevance of both conformations and of a potentially redox-active disulfide bond between the strictly invariant Cys103 and Cys114. The above structural studies focused only on γ-subunit of dsr protein in archaeophilic SRB and clearly shows the lack of studies in α- and β-subunits of thermophilic SRB protein structures.
Graphical representation of compared dissimilatory sulfite reductase structures of (A) D. vulgaris having PDB id 2V4J (Oliveira et al., 2008) and (B) A. fulgidus having PDB id 3C7B (Schiffer et al., 2008) (PDB – www.rcsb.org).
Graphical representation of secondary structures of dissimilatory sulfite reductase subunit chains of Archaeoglobus fulgidus having PDB id 3C7B (1–4 chains; Schiffer et al., 2008), PDB id 1SAU (5 and 6 chains; Weiss et al., 2004), and Desulfovibrio vulgaris having PDB id 2V4J (1–6 chains; Oliveira et al., 2008) (PDB – www.rcsb.org).
Recombinant DNA technology and gene expression have been employed in dsr gene expression and SRB protein structural studies mostly on mesophilic SRB species. Dissimilatory sulfite reductase protein was purified, and the structures were analyzed in D. vulgaris Hildenborough (Pierik, Wolbert, Mutsaers, Hagen, & Veeger, 1992), in hyperthermophilic Archaeon Pyrobaculum islandicum (Molitor et al., 1998), and in D. desulfuricans (Steuber, Arendsen, Hagen, & Kroneck, 1995). Czaja et al. (1995) expressed desulforedoxin (dsr gene) of D. gigas in E. coli and characterized the physical and spectroscopic properties of the recombinant protein. Steuber et al. (1995) studied the molecular properties of the dissimilatory sulfite reductase purified from the membrane of D. desulfuricans and compared with the enzyme from D. vulgaris. Wolfe et al. (1994) found two pairs of [4Fe-4S] and fully metallated siroheme units (stoichiometry Fe/enzyme of 10:1) for their purest desulfoviridin sample from D. vulgaris. Anandkumar, Challaraj Emmanuel, and Maruthamuthu (2008) and Anandkumar et al. (2009a) have expressed the dsr gene of the dissimilatory sulfite reductase protein of thermophilic SRB Desulfotomaculum kuznetsovii and Desulfotomaculum geothermicum and identified with MALDI MS technology.
Therefore, the sulfite reductase subunits, in principle, appeared to be suited to trace the evolution of dissimilatory sulfur metabolism from Archaeons to Eubacteria. Much more structural and functional studies on the enzymes and proteins involved in sulfur metabolism are needed to get insight views on SRB metabolic links.
4 Conclusions
An overview on biotechnological tools implied in SRB studies, physiology and habitats of thermophilic SRB, and theories supporting the corrosion by thermophilic SRB has been presented.
Thermophilic SRB corrosion is a major concern in heat exchangers that interferes in the heat transfer processes. A considerable economy could be saved by reducing bacterial viability in large-scale oil industries with thermostable biocides and corrosion inhibitors at relevant pressure. Regular testing of biocide activity at the particular pressure of the system in which it is to be used would seem a logical amendment to current techniques.
Latest biotechnological tools ought to be employed in the identification and other studies of microbes involved in MIC. Molecular studies on SRB metabolism may shed light on corrosion characteristics of SRB, which in turn help to develop corrosion mitigation procedures. In-depth studies on SRB protein structures may be used in the development of immobilized enzyme sensor probe to detect SRB without cultivable and molecular methods.
The bacterial identification, metabolism, and characteristics of corrosive metabolites of the causative agent of MIC will make the corrosion inhibition strategies easy.
About the authors
Balakrishnan Anandkumar holds an MSc in Microbiology, and a PhD in Chemistry and he has two years of post doctoral experience as a visiting scientist at IGCAR, Kalpakkam, India. He has more than 11 years of research experience in microbiologically influenced corrosion and biofilm control. His interests are the development of molecular biological tools for the identification of microbial groups involved in biofouling of titanium condenser tubes and biofouling control techniques. He has 28 journal papers and 15 conference proceedings in the fields of biofilms and microbial corrosion.
Rani P. George holds an MSc in Botany and a PhD in Botany and having spent two years as a visiting scientist in IGCAR, Kalpakkam, India. She also worked as a Visiting Scientist at Corrosion Protection Centre, UMIST, Manchester, UK during 1998 in the field of MIC probes. She has authored more than 60 journal papers and 30 conference proceedings in the fields of biofouling and corrosion. She has spent 20 years in the field of biofilms and involved in the development of corrosion and biofouling resistant coatings on titanium, stainless steel, low chromium alloys for seawater and humid coastal atmospheric applications.
Sundaram Maruthamuthu holds a Master’s degree and a PhD in Marine Biology. He had worked as a visiting scientist in Dexter, US and as a Brain Pool fellow in South Korea (2012). He has spent 22 years in the fields of Microbial Corrosion and Bioelectro Kinetics, Passivation of stainless steels, Microbial corrosion in petroleum industry, Cathodic protection and microfouling. He has published more than 100 research papers and 50 conference papers. He has completed and also has many organizations sponsored research projects to his credit.
Natarajan Parvathavarthini holds an MSc in Chemistry, an MS in Metallurgical Engineering, and a PhD in Metallurgy. She was a visiting scientist at the Technical Management Concepts, Inc., Wright Patterson Air Force Base, Ohio, USA (1996–1997). She has spent 38 years in the field of localized corrosion such as pitting, crevice, IGC, and hydrogen embrittlement of nuclear structural materials. She has published 121 research papers and 23 design notes for fast reactors.
Uthandi Kamachi Mudali holds an MSc in Materials Science, an MTech in Corrosion Science and Engineering, and a PhD in Metallurgical Engineering. He is a fellow of several international and national societies like NACE International, ASM International, and honorary fellow of the Electrochemical Society of India, etc. He has made excellent contributions to materials development and corrosion control of reactor and reprocessing materials in nuclear industry. He has published 371 papers in journals, co-edited 14 books/proceedings, and holds an H-index of 24. He has guided/coordinated project works of 142 students for their undergraduate, postgraduate, and PhD degrees. He is a Professor at Homi Bhabha National Institute University and an Adjunct Professor at the PSG Institute of Advanced Studies, Coimbatore.
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©2016 by De Gruyter
Articles in the same Issue
- Frontmatter
- In this issue
- Reviews
- Omics-based approaches and their use in the assessment of microbial-influenced corrosion of metals
- Corrosion of multiphase flow pipelines: the impact of crude oil
- Corrosion characteristics of sulfate-reducing bacteria (SRB) and the role of molecular biology in SRB studies: an overview
- Functional coatings formed on the titanium and magnesium alloys as implant materials by plasma electrolytic oxidation technology: fundamental principles and synthesis conditions
- The phosphoric acid industry: equipment, materials, and corrosion
- Original articles
- Electrochemical hydrogen permeation tests under galvanostatic hydrogen charging conditions conventionally used for hydrogen embrittlement study
- A two-stage model based on artificial neural networks to determine pitting corrosion status of 316L stainless steel
Articles in the same Issue
- Frontmatter
- In this issue
- Reviews
- Omics-based approaches and their use in the assessment of microbial-influenced corrosion of metals
- Corrosion of multiphase flow pipelines: the impact of crude oil
- Corrosion characteristics of sulfate-reducing bacteria (SRB) and the role of molecular biology in SRB studies: an overview
- Functional coatings formed on the titanium and magnesium alloys as implant materials by plasma electrolytic oxidation technology: fundamental principles and synthesis conditions
- The phosphoric acid industry: equipment, materials, and corrosion
- Original articles
- Electrochemical hydrogen permeation tests under galvanostatic hydrogen charging conditions conventionally used for hydrogen embrittlement study
- A two-stage model based on artificial neural networks to determine pitting corrosion status of 316L stainless steel
