Sulphate-Reducing Bacteria: Environmental and Engineered Systems

by Larry L. Barton, W. Allan Hamilton

Overview

The sulphate-reducing bacteria (SRB) are a large group of anaerobic organisms that play an important role in many biogeochemical processes. Not only are they of early origins in the development of the biosphere, but their mechanisms of energy metabolism shed light on the limits of life processes in the absence of oxygen. They are widely distributed in nature, and are regular components of engineered systems including, for example, petroleum reservoirs and oil production facilities. SRB are currently subject to extensive genomic studies, which are yielding fresh understanding of their basic biochemical mechanisms, and aiding in the development of novel techniques for the analyses of their environmental roles. This volume provides a timely update on these important microorganisms, from basic science to applications, and will therefore serve as a valuable resource for researchers and graduate students in the fields of microbial ecology, microbial physiology, bioengineering, biogeochemistry and related areas of environmental science.

Product Details

ISBN-13:	9780521123990
Publisher:	Cambridge University Press
Publication date:	12/17/2009
Pages:	552
Product dimensions:	5.90(w) x 8.90(h) x 1.30(d)

About the Author

Larry L. Barton is a Professor in the Department of Biology at the University of New Mexico.

W. Allan Hamilton is Professor Emeritus of Microbiology at the University of Aberdeen.

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Cambridge University Press
978-0-521-85485-6 - Sulphate-reducing Bacteria: Environmental and Engineered Systems - by Larry L. Barton and W. Allan Hamilton
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CHAPTER 1

Energy metabolism and phylogenetic diversity of sulphate-reducing bacteria

Rudolf K. Thauer, Erko Stackebrandt and W. Allan Hamilton

1.1   INTRODUCTION

Sulphate-reducing bacteria (SRB) are those prokaryotic microorganisms, both bacteria and archaea, that can use sulphate as the terminal electron acceptor in their energy metabolism, i.e. that are capable of dissimilatory sulphate reduction. Most of the SRB described to date belong to one of the four following phylogenetic lineages (with some examples of genera): (i) the mesophilic δ-proteobacteria with the genera Desulfovibrio, Desulfobacterium, Desulfobacter, and Desulfobulbus; (ii) the thermophilic Gram-negative bacteria with the genus Thermodesulfovibrio; (iii) the Gram-positive bacteria with the genus Desulfotomaculum; and (iv) the Euryarchaeota with the genus Archaeoglobus (Castro et al., 2000). A fifth lineage, the Thermodesulfobiaceae, has been described recently (Mori et al., 2003).

Many SRB are versatile in that they can use electron acceptors other than sulphate for anaerobic respiration. These include elemental sulphur (Bottcher et al., 2005; Finster et al., 1998), fumarate (Tomei et al., 1995), nitrate (Krekeler and Cypionka, 1995),dimethylsulfoxide (Jonkers et al., 1996), Mn(IV) (Myers and Nealson, 1988) and Fe(III) (Lovley et al., 1993; 2004). Some SRB are even capable of aerobic respiration (Dannenberg et al., 1992; Lemos et al., 2001) although this process appears not to sustain growth, and probably provides these organisms only with energy for maintenance. Since dissimilatory sulphate reduction is inhibited under oxic conditions, SRB can grow at the expense of sulphate reduction only in the complete absence of molecular oxygen. SRB are thus considered to be strictly anaerobic microorganisms and are mainly found in sulphate-rich anoxic habitats (Cypionka, 2000; Fareleira et al., 2003; Sass et al., 1992). These conditions apply in marine sediments since ocean water is rich in sulphate, its concentration being as high as 30 mM. SRB are also present, however, in freshwater sediments, where the sulphate concentration is generally well below 1 mM but is continuously maintained at this level by the re-oxidation of the H₂S to sulphate at the oxic/anoxic interface due to the action of chemolithotrophic and photolithotrophic bacteria (Holmer and Storkholm, 2001). Since most SRB may use electron acceptors other than sulphate, they can also be found in anoxic habitats depleted in sulphate such as the human intestinal tract (Chapter 18). SRB are, however, most abundant in habitats where the availability of sulphate is not limiting.

1.1.2   Thermodynamics

The discussion of the energetics of sulphate reduction is introduced with consideration of the thermodynamic parameters that determine the possible interactions between potential electron donors and sulphate as electron acceptor.

The redox potential, E°′, of the sulphate/HS⁻ couple is −217 mV under standard conditions, which are 1M concentrations of sulphate and HS⁻ at pH 7.0 and 25°C. Under physiological conditions, however, where the concentrations of sulphate are generally < 30 mM and of HS⁻ < 1 mM, the redox potential, E′, is a little more positive and of the order of −200 mV. Thus at all expected concentrations of sulphate and HS⁻, almost any organic compound generated by plants or animals, including carbohydrates, fatty acids, alkanes and aromatic compouds, should, in theory, be able to be completely oxidized to CO₂ since the redox potentials of each of these possible electron donors is significantly more negative than the –200 mV of the sulphate/HS⁻ couple (Table 1.1). Indeed, each of these bio-organic materials has now been shown to be completely mineralized by individual SRB, either alone or in syntrophic association with other organisms. This is even true for methane with a redox potential E°′ of the CO₂/methane couple of −244 mV and therefore a redox potential difference ΔE′ [E′(SO₄²⁻/HS⁻) − E°′(CO₂/CH₄)] of only +44 mV. Remarkably, it has recently been shown that a ΔE′ of +25 mV, equivalent to a free energy change ΔG′of −20 kJ/mol (ΔG′ = −nFΔE′; n = 8) is sufficient to sustain growth of SRB (Hoehler et al., 2001).

For the prediction of electron flow in natural environments, in most cases E°′ rather than E′ of the reductant can be used since the two generally differ by only around 20 mV. There are, however, important exceptions, e.g. the H⁺/H₂ couple and the S°/HS⁻ couple. The redox potential at pH 7.0 (H⁺ concentration constant at 10⁻⁷ M) of the H⁺/H₂ couple increases

Table 1.1. Redox potentials E°′ of electron donors thermodynamically capable and not capable of dissimilatory sulphate, thiosulphate or bisulphite reduction

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Redox couple	n	E°′ (Mv)
2CO2 + 2acetate /hexose	8	−670
CO2 + acetate /pyruvate	2	−660
FeS2/FeS + H2Sd	2	−613
Display matter not available in HTML version	2	−516
CO2/CO	2	−520
Fe2+/Fe°	2	−447
CO2 + acetate/lactate	4	−430
CO2 /formate	2	−432
2H+/H2	2	−414
		(−270 to −300)a
6CO2 /hexose	24	−410
Display matter not available in HTML version	2	−402
CO2 + acetate + NH3/alanine	4	−400
Acetate/ethanol	4	−390
CO2/methanol	6	−370
4CO2 /succinate	12	−312
7CO2 /benzoatee	30	−300
2Acetate/butyrate	4	−290
CO2 + acetate /glycerol	6	−290
2CO2 /acetate	8	−290
4CO2/butyrate	20	−280
3CO2 /propionate	7	−280
N2/NH3f	6	−276
S°/H2S*	2	−270 (−120)b
6CO2/hexaneg	38	−250
CO2/CH4	8	−244
Display matter not available in HTML version	8	−217 (−200)c
SO3H−/HS−	6	−116
Glycine/acetate + NH3	2	−10
Fumarate/succinate	2	+33
Trimethylamine N-oxide/trimethylamine	2	+130
Dimethylsulfoxide/dimethylsulphide	2	+160
Display matter not available in HTML version	1	+200
Display matter not available in HTML version	6	+330
Display matter not available in HTML version	8	+360
Mn4+/Mn2+	2	+407
Display matter not available in HTML version	2	+430
Display matter not available in HTML version	10	+760
O2/2H2O	4	+818
2NO/N2O	2	+1175
H2O2/2H2O	2	+1350
N2O/N2	2	+1.360

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^aCalculated for a H₂ partial pressure of 1 Pa and 10 Pa, respectively.
^bCalculated for a [HS⁻] = 0.1 mM.
^cCalculated for [sulphate] = 30 mM and [HS⁻] = 0.1 mM.
^d(Wächtershäuser, 1992)
^eCalculated from the free energy of formation. ΔG°f of benzoate was estimated from ΔG^°f for benzoic acid (crystalline solid state) (−245 kJ/mol), from the solubility of benzoic acid at 25 °C (27.8 mM) and from the pK of benzoic acid (4.2) to be –212.3  kJ/mol (Thauer and Morris, 1984).
^fN₂ cannot be used as electron acceptor for energy conservation because of the too high energy of activation required for its reduction.
^g(Zengler et al., 1999)
^h(Ehrenreich and Widdel, 1994)
Notes: E^°′ at pH 7.0 are given for H₂, CO₂, CO, CH₄ and O₂ in the gaseous state at 10⁵ Pa, for S^° in the solid state and for all other compounds in aqueous solution at 1M concentration. The values in brackets are E′ values calculated for physiological substrate and product concentrations. E^°′ values were calculated from ΔG^°′ values: ΔG^°′ = −nFΔE, where n is the number of electrons and F = 96 487 J/mol/volt. Except were indicated, ΔG^°′ values were taken from (Thauer et al., 1977).

from −414 mV at an H₂ partial pressure of 10⁵ Pa (standard condition) to values between –270 mV and –300 mV at H₂ partial pressures between 1 and 10 Pa, which is the concentration range of H₂ prevailing in sediments. Thus the oxidation of acetate to CO₂ (E°′=  −290 mV) with H⁺ as electron acceptor (E′= −270 mV at 1 Pa:H₂) becomes thermodynamically feasible and there are organisms that appear to live at the expense of this equation (Galouchko and Rozanova, 1996; Lee and Zinder, 1988; Shigematsu et al., 2004).

CH₃COO⁻ + H⁺ + 2H₂O = 2CO₂ + 4H₂   ΔG°′ = + 95 kJ mol  (1.1)

The redox potential of the S°/HS⁻ couple (S° in the solid state and therefore constant) increases from –270 mV under standard conditions to −120 mV under physiological conditions where the HS⁻ concentrations can be 0.1 mM or even lower. As a consequence, under in situ conditions the reduction of sulphate with H₂S to S° is endergonic. In agreement with this prediction, SRB have been found that can grow at the expense of S° disproportionation to sulphate and HS⁻ (Finster et al., 1998):

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1.1.3   Energy coupling

Growth of SRB with dissimilatory sulphate reduction indicates that substrate oxidation is coupled with adenosine triphosphate (ATP) synthesis from adenosine diphosphate (ADP) and inorganic phosphate. It leaves open, however, whether coupling is by substrate level phosphorylation and/or electron transport-linked phosphorylation (Thauer et al., 1977). In substrate level phosphorylation an "energy-rich" intermediate is formed from organic substrates during exergonic oxidation reactions. The "energy-rich" intermediate is generally an acyl phosphate or an acyl thioester, which have group transfer potentials equivalent to that of ATP, and are in an enzyme-catalyzed equilibrium with the ADP/ATP system. In electron transport-linked phosphorylation the redox potential difference between electron carriers and the terminal electron acceptor is conserved in a transmembrane electrochemical proton or sodium ion gradient, which drives the phosphorylation of ADP via a membrane-bound ATP synthase.

For many years it was thought that it was only possible to grow SRB on organic substrates as electron donors for dissimilatory sulphate reduction, and this led to the belief that in these organisms energy is conserved mainly or exclusively via substrate level phosphorylation. However, in 1978 it was unambiguously shown that Desulfovibrio vulgaris can grow with H₂ and sulphate as the sole energy source (Badziong and Thauer, 1978).

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During growth on H₂ and sulphate, energy must be conserved by electron transport-linked phosphorylation since substrate level phosphorylation is only possible when the substrate oxidized is organic. There is, however, an exception to this general rule. The oxidation of bisulphite to sulphate can be coupled by substrate level phosphorylation via an energy-rich adenosine phosphosulphate (APS) intermediate. Using this reaction some SRB can grow at the expense of bisulphite disproportionation to sulphate and hydrogen sulphide (Bak and Cypionka, 1987; Frederiksen and Finster, 2003; Kramer and Cypionka, 1989).

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This chapter first summarizes what is presently known about the biochemistry of dissimilatory sulphate reduction with H₂. Thermodynamic problems associated with the sulphate-dependent oxidations of substrates other than H₂ are then outlined. Subsequently, also under energetic aspects, the trophic interactions of SRB with other microorganisms in their habitats are described. Finally, the phylogenetic diversity of SRB is discussed.

Some of the arguments that will be put forward are based on genome sequence information. Until now, only the genome sequences of three SRB, of Archaeoglobus fulgidus (Klenk et al., 1997), of Desulfovibrio vulgaris (Hildenborough) (Heidelberg et al., 2004; Hemme and Wall, 2004) and Desulfotalea psychrophila (Rabus et al., 2004), have been published. The genomes of many other SRB with different metabolic capacities and from different phylogenetic origins are presently being sequenced. Only when we have these data will we have a complete picture of the energy metabolism of SRB (Chapter 3).

For a previous review on the bioenergetic strategies of sulphate-reducing bacteria see Peck (1993).

1.2   DISSIMILATORY SULPHATE REDUCTION WITH H₂

The equations and proteins involved in dissimilatory sulphate reduction with H₂ will be described for Desulfovibrio vulgaris (Hansen, 1994; Matias et al., 2005). The biochemistry of this δ-proteobacterium and of closely related species has been studied in detail and the genome sequence of the Hildenborough strain has recently been published (Heidelberg et al., 2004). Most of the results can probably be generalized to other SRB capable of growth on H₂ as sole energy source such as D. desulfuricans, Thermodesulphobacterium commune, Desulfobacterium autotrophicus, Desulfotomaculum orientis and Archaeoglobus profundus.

1.2.1   Sulphate activation

Dissimilatory sulphate reduction with H₂ to H₂S in D. vulgaris proceeds via HSO₃⁻ as intermediate. The redox potential, E°′, of the SO₄²⁻/HSO₃⁻ couple is −516 mV and thus more than 100 mV more negative that of the H⁺/H₂ couple (Table 1.1). Reduction of sulphate to bisulphite with H₂ can therefore only proceed after some input of energy. It has been shown that sulphate is first activated with ATP to adenosine phosphosulphate (= adenylylsulphate) (APS), and that the redox potential of the resulting APS/HSO₃⁻ couple is −60 mV. The reaction is catalyzed by ATP sulphurylase (Sperling et al., 1998; Taguchi et al., 2004) and consumes the energy of up to two enegy-rich bonds.

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Desulfovibrio contain an active cytoplasmic inorganic pyrophosphatase that probably catalyzes the hydrolysis of most of the inorganic pyrophosphate generated in reaction 1.5 (Kobayashi et al., 1975; Liu and Legall, 1990; Ware and Postgate, 1971; see also Weinberg et al., 2004). Based on the genome sequence of D. vulgaris, there is no evidence of a membrane-associated inorganic pyrophosphatase which would allow conservation of part of the energy released during pyrophosphate hydrolysis in the form of a transmembrane electrochemical proton potential, thus reducing somewhat the energy cost of sulphate activation.

1.2.2   Cytoplasmic APS reduction

The sulphate activation to APS increases the redox potential of the first step in dissimilatory sulphate reduction from −516 mV to −60 mV. This is well above the redox potential of the H⁺/H₂ couple and allows the reduction with H₂ to proceed even at low H₂ concentrations. Desulfovibrio contain a cytoplasmic APS reductase (= adenylylsulphate reductase) whose direct electron donor is not yet known (Fritz et al., 2002; Kremer and Hansen, 1988; Lopez-Cortes et al., 2005; Yagi and Ogata, 1996).

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1.2.3   Cytoplasmic bisulphite reduction

The reduction of APS to HSO₃⁻ is followed by the reduction of HSO₃⁻ to HS⁻, a reaction catalyzed by a cytoplasmic bisulphite reductase (Crane et al., 1997; Friedrich, 2002; Kremer and Hansen, 1988; Larsen et al., 1999; Steger et al., 2002; Zverlov et al., 2005), whose direct electron donor has also still to be identified. For assay of enzyme activity reduced viologen dyes are generally used.

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With respect to the mechanism of this equation, there has been considerable controversy over the last 30 years, which is not yet completely resolved. One of the reasons for this is that bisulphite reductase also catalyzes reactions 1.8b and 1.8c when the HSO₃⁻ concentration is high and the reductant concentration is limiting (Akagi, 1995). SRB contain a thiosulphate reductase which catalyzes equation 1.9.

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Thus bisulphite reduction could proceed in three two-electron steps rather than in one six-electron step, especially when SRB are grown with bisulphite or thiosulphate rather than sulphate as terminal electron acceptor (Fitz and Cypionka, 1990; Sass et al., 1992). However, recently it has been shown that when D. vulgaris is genetically impaired in thiosulphate reduction, this does not affect its ability to grow on sulphate and H₂ (Broco et al., 2005). This is interpreted as indicating that, at least under these growth conditions, bisulphite is reduced in a single step. In the following, it is therefore assumed that APS and HSO₃⁻ are the only intermediary electron acceptors involved in dissimilatory sulphate reduction with H₂.

1.2.4   Periplasmic H₂ oxidation

D. vulgaris contains four periplasmic hydrogenases, three [NiFe]-hydrogenases and one [FeFe]-hydrogenase: of these, three hydrogenases couple with the major periplasmic poly-heme cytochrome c (TpI-c3), and one, the [NiFe]-hydrogenases 2, most probably with a second poly-heme cytochrome c (TpII-c3) (Heidelberg et al., 2004; Matias et al., 2005). When the organism is grown on H₂ and sulphate in medium depleted in nickel, only the [FeFe]-hydrogenase is synthesized without this having a noticeable effect on the growth rate (R. K. Thauer, unpublished results). Growth of D. vulgaris is also not impaired when the genes for the [FeFe]-hydrogenase (Haveman et al., 2003; Pohorelic et al., 2002) or one of the NiFe hydrogenases (Goenka et al., 2005) are deleted. These findings indicate that the four hydrogenases can fully functionally replace each other, at least under the growth conditions employed in the laboratory where the H₂ concentration in the fermenters is kept high.

1.2.5   Transmembrane electron transport

Coupling of periplasmic hydrogen oxidation with cytoplasmic APS and HSO₃⁻ reduction must involve electron transport through the cytoplasmic membrane. The electron transport is most probably catalyzed by the Hmc complex, which is associated on the periplasmic side with a poly-heme cytochrome c, and on the cytoplasmic side with an iron-sulphur protein with sequence similarity to heterodisulphide reductase (Keon and Voordouw, 1996; Matias et al., 2005; Rossi et al., 1993). D. vulgaris deleted in the hmc genes grew normally on lactate and sulphate, but growth on H₂ and sulphate was hampered (Dolla et al., 2000; Haveman et al., 2003; Keon and Voordouw, 1996). The genome of D. vulgaris harbours two other polycistronic transcription units predicted to encode for transmembrane protein complexes (TpII-c₃ and Hme), associated on the periplasmic side with a cytochrome c and on the cytoplasmic side with an iron-sulphur protein, again with sequence similarity to heterodisulphide reductase (Heidelberg et al., 2004; Matias et al., 2005). The Hme genes are part of a locus that includes the genes for bisulphite reductase. The three transmembrane complexes Hmc, Hme and TpII-c₃ could have overlapping functions, in a like manner to the four periplasmic hydrogenases. In the genome, a further gene cluster for a transmembrane protein complex is found which lacks the periplasmic cytochrome c (Qmo complex) (Pires et al., 2003). There is indirect evidence that the Qmo complex is involved in APS reduction (Matias et al., 2005).

Heterodisulphide reductase from methanogens catalyzes the reduction of the heterodisulphide CoM-S-S-CoB to coenzyme M (HS-CoM) and coenzyme B (HS-CoB) (Hedderich et al., 1998). Both coenzymes are absent from SRB, and cell extracts of SRB neither catalyze the reduction of CoM-S-S-CoB nor the oxidation of CoM-SH plus CoB-SH (Mander et al., 2002; 2004). The iron-sulphur proteins in SRB with sequence similarity to heterodisulphide reductase must therefore have a different substrate specificity and/or a different function. However, since in methanogenic archaea heterodisulfide reduction links H₂ oxidation with methyl-coenzyme M reduction to methane, it is tempting to speculate that in SRB a disulphide/–SH couple might also be involved in the electron transport from H₂ to HSO₃⁻.

1.2.6   ATP synthesis and sulphate transport

As indicated above, up to two ATP equivalents are required to activate sulphate before it can be reduced to HSO₃⁻. The reduction of HSO₃⁻ to HS⁻ must therefore be coupled with the phosphorylation of at least 2 mol ADP in order that the SRB can grow on H₂ and sulphate. Growth yield data, extrapolated to infinite growth rates, for D. vulgaris on H₂ and sulphate were 12.2 g/mol sulphate, and on H₂ and thiosulphate 33.5 g/mol, indicating that HSO₃⁻ reduction with H₂ to HS⁻ is coupled with the net synthesis of approximately three ATP (Badziong and Thauer, 1978). In the interpretation of these growth yield data it has to be considered that sulphate must be transported into the cells before it can be reduced and that this transport also requires energy. Available evidence indicates that sulphate is symported with three protons (Cypionka, 1987; Kreke and Cypionka, 1992), or three sodium ions (Kreke and Cypionka, 1994) which is probably equivalent to the consumption of one third or one fourth of an ATP, as discussed below.

1.2.7   Proton stoichiometries

D. vulgaris contains a F₀F₁-type proton-translocating ATPase/ATP synthase (Heidelberg et al., 2004; Hemme and Wall, 2004) of as yet unknown H⁺ to ATP stoichiometry. Recent structural analyses of F₀F₁ ATPases from different organisms indicates that the H⁺ to ATP stoichiometry may differ from organism to organism, and may be as high as five or as low as three in some organisms (Dimroth and Cook, 2004; Meier et al., 2005; Mueller, 2004; Murata et al., 2005). If the enzyme in D. vulgaris has a stoichiometry of three protons per ATP, then at least nine electrogenic protons are required for the synthesis of the three ATP predicted from growth yields to be formed during bisulphite reduction to HS⁻. If the stoichiometry is five protons per ATP, then fifteen protons are required. Of these, six are generated from H₂ in the periplasm in a scalar reaction catalyzed by the periplasmic hydrogenases. The other protons required for ATP synthesis must therefore be generated during bisulphite reduction with H₂ by electrogenic proton translocation from the cytoplasm to the periplasm. Although menaquinone is the major quinone found in the cytoplasmic membrane of all SRB, its involvement in this proton translocation is unlikely since the redox potential, E°′, of the menaquinone ox/red couple is −74 mV and thus more positive than that of the HSO₃⁻/HS⁻ couple (−116 mV).

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© Cambridge University Press

Table of Contents

Preface; 1. Energy metabolism and phylogenetic diversity of sulphate-reducing bacteria Rudolf K. Thauer, Erko Stackebrandt and W. Allan Hamilton; 2. Molecular strategies for studies of natural populations of sulphate-reducing micro-organisms David A. Stahl, Alexander Loy and Michael Wagner; 3. Functional genomics of sulphate-reducing prokaryotes Ralf Rabus and Axel Strittmatter; 4. Evaluation of stress response in sulphate-reducing bacteria through genome analysis J. D. Wall, H. C. Bill Yen, and E. C. Drury; 5. Response of sulphate-reducing bacteria to oxygen Henrik Sass and Heribert Cypionka; 6. Biochemical, proteomic and genetic characterisation of oxygen survival mechanisms in sulphate-reducing bacteria of the genus Desulfovibrio Alain Dolla, Donald M. Kurtz, Jr., Miguel Teixeira and Gerrit Voordouw; 7. Biochemical, genetic and genomic characterisation of anaerobic electron transport pathways in sulphate-reducing Δ-proteobacteria Inês A. C. Pereira, Shelley A. Haveman and Gerrit Voordouw; 8. Dissimilatory nitrate and nitrite ammonification by sulphate-reducing eubacteria José J. G. Moura, Pablo Gonzalez, Isabel Moura and Guy Fauque; 9. Anaerobic degradation of hydrocarbons with sulphate as electron acceptor Friedrich Widdel, Florin Musat, Katrin Knittel and Alexander Galushko; 10. Sulphate-reducing bacteria from oil field environments and deep-sea hydrothermal vents Bernard Ollivier, Jean-Luc Cayol and Guy Fauque; 11. The sub-seafloor biosphere and sulphate-reducing prokaryotes: their presence and significance R. John Parkes and Henrik Sass; 12. Eco-physiology of sulphate-reducing bacteria in environmental biofilms Satoshi Okabe; 13. Bioprocess engineering of sulphate reduction for environmental technology Piet N. L. Lens, Marcus Vallero and Giovanni Esposito; 14. Bioremediation of metals and metalloids by precipitation and cellular binding Simon L. Hockin and Geoffrey M. Gadd; 15. Enzymatic and genomic studies on the reduction of mercury and selected metallic oxy-anions by sulphate-reducing bacteria Mireille Bruschi, Larry L. Barton, Florence Goulhen, and Richard M. Plunkett; 16. Sulphate-reducing bacteria and their role in corrosion of ferrous materials Iwona B. Beech and Jan A. Sunner; 17. Anaerobic metabolism of nitroaromatic compounds and bioremediation of explosive by sulphate-reducing bacteria Raj Boopathy; 18. Sulphate-reducing bacteria and the human large intestine George T. Macfarlane, John H. Cummings and Sandra Macfarlan.

Editorial Reviews

Review of the hardback: 'It is an essential reference for microbiologists and global ecosystem researchers, and is recommended as a priority purchase for libraries, and by individuals whose work relates to SRB. The quality of the science and presentation is excellent, and a joy to read.' Ann Wood, King's College London

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