How sulphate-reducing microorganisms cope with stress: lessons from systems biology (original) (raw)

• Weber, H., Polen, T., Heuveling, J., Wendisch, V. F. & Hengge, R. Genome-wide analysis of the general stress response network in Escherichia coli: σS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187, 1591–1603 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Storz, G. & Hengge-Aronis, R. Bacterial Stress Responses (ASM Press, Washington DC, 2000).
  Google Scholar
• Hecker, M. & Völker, U. General stress response of Bacillus subtilis and other bacteria. Adv. Microb. Physiol. 44, 35–91 (2001).
  Article CAS PubMed Google Scholar
• Hecker, M., Pané-Farré, J. & Völker, U. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 61, 215–236 (2007).
  Article CAS PubMed Google Scholar
• Estruch, F. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol. Rev. 24, 469–486 (2000).
  Article CAS PubMed Google Scholar
• Alm, E., Huang, K. & Arkin, A. The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLoS Comput. Biol. 2, e143 (2006). This study shows that most of the recently acquired histidine kinases in D. vulgaris have arisen by lineage-specific expansion, and that these genes are more likely to be present as orphans, separate from their cognate partner.
  Article PubMed PubMed Central CAS Google Scholar
• Muyzer, G. & Stams, A. J. M. The ecology and biotechnology of sulphate-reducing bacteria. Nature Rev. Microbiol. 6, 441–454 (2008).
  Article CAS Google Scholar
• Barton, L. L. & Fauque, G. D. Advances in Applied Microbiology Ch. 2 (eds Allen I. Laskin, S. S. & Geoffrey, M. G.) 68, 41–98 (Academic, New York, 2009).
  Google Scholar
• Postgate, J. R. The Sulphate Reducing Bacteria (Cambridge Univ. Press, Cambridge, UK, 1984).
  Google Scholar
• Voordouw, G. The genus Desulfovibrio: the Centennial. Appl. Environ. Microbiol. 61, 2813–2819 (1995).
  CAS PubMed PubMed Central Google Scholar
• Baumgartner, L. K. et al. Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sediment. Geol. 185, 131–145 (2006).
  Article CAS Google Scholar
• Goldstein E. J. C., Citron, D. M., Peraino, V. A. & Cross, S. A. Desulfovibrio desulfuricans bacteremia and review of human Desulfovibrio infections. J. Clin. Microbiol. 41, 2752–2754 (2003).
  Article PubMed PubMed Central Google Scholar
• Cardenas, E. et al. Significant association between sulfate-reducing bacteria and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach. Appl. Environ. Microbiol. 76, 6778–6786 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Coetser, S. E. & Cloete, T. E. Biofouling and biocorrosion in industrial water systems. Crit. Rev. Microbiol. 31, 213–232 (2005).
  Article CAS PubMed Google Scholar
• He, Z. et al. GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J. 1, 67–77 (2007). A description of the first comprehensive functional gene array, GeoChip 2.0, and its application for tracking the dynamics of metal-reducing bacteria during in situ bioremediation of a uranium-contaminated site.
  Article CAS PubMed Google Scholar
• Dinh, H. T. et al. Iron corrosion by novel anaerobic microorganisms. Nature 427, 829–832 (2004).
  Article CAS PubMed Google Scholar
• Nemati, M., Jenneman, G. E. & Voordouw, G. Impact of nitrate-mediated microbial control of souring in oil reservoirs on the extent of corrosion. Biotechnol. Prog. 17, 852–859 (2001).
  Article CAS PubMed Google Scholar
• Hao, O. J., Chen, J. M., Huang, L. & Buglass, R. L. Sulfate-reducing bacteria. Crit. Rev. Environ. Sci. Tech. 26, 155–187 (1996).
  Article CAS Google Scholar
• Satoh, H., Odagiri, M., Ito, T. & Okabe, S. Microbial community structures and in situ sulfate-reducing and sulfur-oxidizing activities in biofilms developed on mortar specimens in a corroded sewer system. Water Res. 43, 4729–4739 (2009).
  Article CAS PubMed Google Scholar
• Wall, J. D. & Krumholz, L. R. Uranium reduction. Annu. Rev. Microbiol. 60, 149–166 (2006).
  Article CAS PubMed Google Scholar
• Valls, M. & de Lorenzo, V. Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol. Rev. 26, 327–338 (2002).
  Article CAS PubMed Google Scholar
• Klonowska, A. et al. Hexavalent chromium reduction Desulfovibrio vulgaris Hildenborough causes transitory inhibition of sulfate reduction and cell growth. Appl. Microbiol. Biotechnol. 78, 1007–1016 (2008).
  Article CAS PubMed Google Scholar
• Rabus, R., Hansen, T. & Widdel, F. in The Prokaryotes. A Handbook on the Biology of Bacteria: Proteobacteria: Gamma subclass 3rd edn Vol. 2 Ch. 1.22 (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stakebrandt, E.) 659–678 (Springer, New York, 2006).
  Google Scholar
• Heidelberg, J. F. et al. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nature Biotech. 22, 554–559 (2004). A keystone paper describing the first genome to be sequenced from a sulphate-reducing bacterium.
  Article CAS Google Scholar
• Klenk, H. P. et al. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364–370 (1997).
  Article CAS PubMed Google Scholar
• Rabus, R. et al. The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environ. Microbiol. 6, 887–902 (2004).
  Article CAS PubMed Google Scholar
• Nakazawa, H. et al. Whole genome sequence of Desulfovibrio magneticus strain RS-1 revealed common gene clusters in magnetotactic bacteria. Genome Res. 19, 1801–1808 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Strittmatter, A. W. et al. Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide. Environ. Microbiol. 11, 1038–1055 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Junier, P. et al. The genome of the Gram-positive metal- and sulfate-reducing bacterium Desulfotomaculum reducens strain MI-1. Environ. Microbiol. 12, 2738–2754 (2010).
  CAS PubMed PubMed Central Google Scholar
• Spring, S. et al. Complete genome sequence of Desulfotomaculum acetoxidans type strain (5575T). Stand. Genomic. Sci. 1, 242–253 (2009).
  Article PubMed PubMed Central Google Scholar
• Chivian, D. et al. Environmental genomics reveals a single-species ecosystem deep within earth. Science 322, 275–278 (2008).
  Article CAS PubMed Google Scholar
• Thauer, R. K., Stackebrandt, E. & Hamilton, W. A. in Sulphate-Reducing Bacteria: Environmental and Engineered Systems Ch.1 (Cambridge Univ. Press, Cambridge, UK, 2007). An excellent summary of the energetics of sulphate reduction by bacteria.
  Google Scholar
• Odom, J. M. & Peck, H. D. Jr. Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria, Desulfovibrio sp. FEMS Microbiol. Lett. 12, 47–50 (1981). The first description of the hydrogen-cycling hypothesis.
  Article CAS Google Scholar
• Voordouw, G. Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 184, 5903–5911 (2002). This article provides a significant update to the hydrogen-cycling hypothesis based on genomic-sequence data and the identification of putative cytoplasmic hydrogenases.
  Article CAS PubMed PubMed Central Google Scholar
• Rossi, M. et al. The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex. J. Bacteriol. 175, 4699–4711 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Zane, G. M., Yen, H. C. & Wall, J. D. Effect of the deletion of qmoABC and the promoter distal gene encoding a hypothetical protein on sulfate-reduction in Desulfovibrio vulgaris Hildenborough. Appl. Environ. Microbiol. 76, 5500–5509. (2010).
  Google Scholar
• Mukhopadhyay, A. et al. Salt stress in Desulfovibrio vulgaris Hildenborough: an integrated genomics approach. J. Bacteriol. 188, 4068–4078 (2006). A comprehensive use of data from various functional genomic studies beyond transcriptomics and proteomics to elucidate the cellular response to stress conditions.
  Article CAS PubMed PubMed Central Google Scholar
• He, Z. et al. Global transcriptional, physiological, and metabolite analyses of the responses of Desulfovibrio vulgaris Hildenborough to salt adaptation. Appl. Environ. Microbiol. 76, 1574–1586 (2010).
  Article CAS PubMed Google Scholar
• He, Q. et al. Impact of elevated nitrate on sulfate-reducing bacteria: a comparative study of Desulfovibrio vulgaris. ISME J. 4, 1386–1397 (2010).
  Article CAS PubMed Google Scholar
• He, Q. et al. Energetic consequences of nitrite stress in Desulfovibrio vulgaris Hildenborough, inferred from global transcriptional analysis. Appl. Environ. Microbiol. 72, 4370–4381 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Pereira, P. et al. Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis. Antonie Van Leeuwenhoek 93, 347–362 (2008).
  Article CAS PubMed Google Scholar
• Galperin, M. Y. Diversity of structure and function of response regulator output domains. Curr. Opin. Microbiol. 13, 150–159 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Galperin, M. Y., Higdon, R. & Kolker, E. Interplay of heritage and habitat in the distribution of bacterial signal transduction systems. Mol. Biosyst. 6, 721–728 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Ulrich, L. E., Koonin, E. V. & Zhulin, I. B. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13, 52–56 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Mascher, T., Helmann, J. D. & Unden, G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70, 910–938 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Rodionov, D., Dubchak, I., Arkin, A., Alm, E. & Gelfand, M. Reconstruction of regulatory and metabolic pathways in metal-reducing δ-proteobacteria. Genome Biol. 5, R90 (2004).
  Article PubMed PubMed Central Google Scholar
• Rodionov, D. A., Dubchak, I. L., Arkin, A. P., Alm, E. J. & Gelfand, M. S. Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput. Biol. 1, e55 (2005).
  Article PubMed PubMed Central CAS Google Scholar
• Mukhopadhyay, A. et al. Cell-wide responses to low-oxygen exposure in Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 189, 5996–6010 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Pereira, P. et al. Transcriptional response of Desulfovibrio vulgaris Hildenborough to oxidative stress mimicking environmental conditions. Arch. Microbiol. 189, 451–461 (2008).
  Article CAS PubMed Google Scholar
• Zhang, W., Culley, D. E., Hogan, M., Vitiritti, L. & Brockman, F. J. Oxidative stress and heat-shock responses in Desulfovibrio vulgaris by genome-wide transcriptomic analysis. Antonie Van Leeuwenhoek 90, 41–55 (2006).
  Article CAS PubMed Google Scholar
• Zhou, A. et al. Hydrogen peroxide-induced oxidative stress responses in Desulfovibrio vulgaris Hildenborough. Environ. Microbiol. 12, 2645–2657 (2010).
  CAS PubMed Google Scholar
• Haveman, S. A., Greene, E. A., Stilwell, C. P., Voordouw, J. K. & Voordouw, G. Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J. Bacteriol. 186, 7944–7950 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Chhabra, S. R. et al. Global analysis of heat shock response in Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 188, 1817–1828 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Clark, M. E. et al. Temporal transcriptomic analysis as Desulfovibrio vulgaris Hildenborough transitions into stationary phase during electron donor depletion. Appl. Environ. Microbiol. 72, 5578–5588 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Stolyar, S. et al. Response of Desulfovibrio vulgaris to alkaline stress. J. Bacteriol. 189, 8944–8952 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Hazen, T. C. & Stahl, D. A. Using the stress response to monitor process control: pathways to more effective bioremediation. Curr. Opin. Biotechnol. 17, 285–290 (2006).
  Article CAS PubMed Google Scholar
• Durfee, T. et al. The complete genome sequence of Escherichia coli DH10B: insights into the biology of a laboratory workhorse. J. Bacteriol. 190, 2597–2606 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Lobo, S. A., Melo, A. M., Carita, J. N., Teixeira, M. & Saraiva, L. M. The anaerobe Desulfovibrio desulfuricans ATCC 27774 grows at nearly atmospheric oxygen levels. FEBS Lett. 581, 433–436 (2007).
  Article CAS PubMed Google Scholar
• Cypionka, H. Oxygen respiration by Desulfovibrio species. Annu. Rev. Microbiol. 54, 827–848 (2000).
  Article CAS PubMed Google Scholar
• Coulter, E. D. & Kurtz, D. M. A role for rubredoxin in oxidative stress protection in Desulfovibrio vulgaris: catalytic electron transfer to rubrerythrin and two-iron superoxide reductase. Arch. Biochem. Biophys. 394, 76–86 (2001).
  Article CAS PubMed Google Scholar
• Lumppio, H. L., Shenvi, N. V., Summers, A. O., Voordouw, G. & Kurtz, D. M. Jr. Rubrerythrin and rubredoxin oxidoreductase in Desulfovibrio vulgaris: a novel oxidative stress protection system. J. Bacteriol. 183, 101–108 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Fournier, M. et al. Function of oxygen resistance proteins in the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 185, 71–79 (2003).
  Article PubMed PubMed Central CAS Google Scholar
• Jenney, F. E. Jr. et al. Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286, 306–309 (1999).
  Article CAS PubMed Google Scholar
• Arnér, E. S. J. & Holmgren, A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102–6109 (2000).
  Article PubMed Google Scholar
• Storz, G. & Imlayt, J. A. Oxidative stress. Curr. Opin. Microbiol. 2, 188–194 (1999).
  Article CAS PubMed Google Scholar
• Lee, J. W. & Helmann, J. D. The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440, 363–367 (2006).
  Article CAS PubMed Google Scholar
• Lee, J. W. & Helmann, J. Functional specialization within the Fur family of metalloregulators. Biometals 20, 485–499 (2007).
  Article CAS PubMed Google Scholar
• Jozefczuk, S. et al. Metabolomic and transcriptomic stress response of Escherichia coli. Mol. Syst. Biol. 6, 364 (2010).
  Article PubMed PubMed Central Google Scholar
• Mitchell, A. et al. Adaptive prediction of environmental changes by microorganisms. Nature 460, 220–224 (2009).
  Article CAS PubMed Google Scholar
• Kapfhammer, D. et al. Role for glycine betaine transport in Vibrio cholerae osmoadaptation and biofilm formation within microbial communities. Appl. Environ. Microbiol. 71, 3840–3847(2005).
  Article CAS PubMed PubMed Central Google Scholar
• Ko, R., Smith, L. T. & Smith, G. M. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J. Bacteriol. 176, 426–431 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Bender, K. S. et al. Analysis of a ferric uptake regulator (Fur) mutant of Desulfovibrio vulgaris Hildenborough. Appl. Environ. Microbiol. 73, 5389–5400 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, W., Culley, D., Nie, L. & Scholten, J. Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface. Appl. Microbiol. Biotechnol. 76, 447–457 (2007).
  Article CAS PubMed Google Scholar
• Elias, D. A. et al. Expression profiling of hypothetical genes in Desulfovibrio vulgaris leads to improved functional annotation. Nucleic Acids Res. 37, 2926–2939 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Stams, A. J. M. & Plugge, C. M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Rev. Microbiol. 7, 568–577 (2009). A recent review describing the discovery, diversity and energetics of syntrophy.
  Article CAS Google Scholar
• Bryant, M. P et al. Growth of Desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl. Environ. Microbiol. 33, 51162–51169 (1977).
  Google Scholar
• Stolyar, S. et al. Metabolic modeling of a mutualistic microbial community. Mol. Syst. Biol. 3, 92 (2007). An early example of the extension of flux balance modelling to a microbial community.
  Article PubMed PubMed Central CAS Google Scholar
• Walker, C. B. et al. The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J. Bacteriol. 191, 5793–5801 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Whitman, W. B., Shieh, J., Sohn, S., Caras, D. S. & Premachandran, U. Isolation and characterization of 22 mesophilic methanococci. Syst. Appl. Microbiol. 7, 235–240 (1986).
  Article Google Scholar
• Endler, J. A. Natural Selection in the Wild (Princeton Univ. Press, Princeton, 1986).
  Google Scholar
• Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991).
  Google Scholar
• Thompson, J. N. Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329–332 (1998).
  Article CAS PubMed Google Scholar
• May, R. M. Theoretical Ecology: Principles and Applications 49–71 (Saunders, Philadelphia, 1976). The presentation of the first ecological model to be developed for mutually beneficial interactions between species. This model predicts that mutualistic associations will be unstable because they are pushed to unsustainable levels of growth.
  Google Scholar
• Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull., J. J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004).
  Article PubMed Google Scholar
• Shou, W., Ram, S. & Vilar, J. M. G. Synthetic cooperation in engineered yeast populations. Proc. Natl Acad. Sci. USA 104, 1877–1882 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Hillesland, K. L. & Stahl, D. A. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl Acad. Sci. USA 107, 2124–2129 (2010). The first example of syntrophy evolution observed in real time. This paper is a good example of how research on a Desulfovibrio sp. model system can both affect microbiology and address broad questions in evolutionary biology.
  Article CAS PubMed PubMed Central Google Scholar
• Miller, L. D. et al. Establishment and metabolic analysis of a model microbial community for understanding trophic and electron accepting interactions of subsurface anaerobic environments. BMC Microbiol. 10, 149 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Shaikh, A. S., Tang, Y. J., Mukhopadhyay, A. & Keasling, J. D. Isotopomer distributions in amino acids from a highly expressed protein as a proxy for those from total protein. Anal. Chem. 80, 886–890 (2008). This study develops a strategy that allows the use of isotopomer-based flux analysis to study mixed cultures, such as the D. vulgaris H.– M. maripaludis co-culture.
  Google Scholar
• Breitbart, M. et al. Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Ciénegas, Mexico. Environ. Microbiol. 11, 16–34 (2009).
  Article CAS PubMed Google Scholar
• Biddle, J. F., Fitz-Gibbon, S., Schuster, S. C., Brenchley, J. E. & House, C. H. Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment Proc. Natl Acad. Sci. USA 105, 10583–10588 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Hu, Y. et al. Construction and preliminary analysis of a deep-sea sediment metagenomic fosmid library from Qiongdongnan Basin, South China Sea. Mar. Biotechnol. 12, 719–727 (2010).
  Article CAS Google Scholar
• Woyke, T. et al. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950–955 (2006).
  Article CAS PubMed Google Scholar
• Pernthaler, A. et al. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc. Natl Acad. Sci. USA 105, 7052–7057 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Warnecke, F. et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560–565 (2007).
  Article CAS PubMed Google Scholar
• Brulc, J. M. et al. Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl Acad. Sci. USA 106, 1948–1953 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Hemme, C. L. et al. Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J. 4, 660–672 (2010). The first community-level analysis to document the impact of anthropogenic change on microbial communities and to demonstrate the importance of lateral gene transfer in the adaptation of a microbial community to environmental change.
  Article CAS PubMed Google Scholar
• Meyer, B. & Kuever, J. Molecular analysis of the diversity of sulfate-reducing and sulfur-oxidizing prokaryotes in the environment using aprA as functional marker gene. Appl. Environ. Microbiol. 73, 7664–7679 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Karkhoff-Schweizer, R., Huber, D. & Voordouw, G. Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR. Appl. Environ. Microbiol. 61, 290–296 (1995).
  CAS PubMed PubMed Central Google Scholar
• Wagner, M., Roger, A. J., Flax, J. L., Brusseau, G. A. & Stahl, D. A. Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J. Bacteriol. 180, 2975–2982 (1998). This paper develops the general approach for using the dsrAB genes to characterize the diversity of natural populations of sulphate-reducing microorganisms. Many of the sequences on the GeoChip were derived from these environmental sequences.
  CAS PubMed PubMed Central Google Scholar
• Dar, S. A., Kuenen, J. G. & Muyzer, G. Nested PCR-denaturing gradient gel electrophoresis approach to determine the diversity of sulfate-reducing bacteria in complex microbial communities. Appl. Environ. Microbiol. 71, 2325–2330 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Moreau, J. W., Zierenberg, R. A. & Banfield, J. F. Diversity of dissimilatory sulfite reductase genes (dsrAB) in a salt marsh impacted by long-term acid mine drainage. Appl. Environ. Microbiol. 76, 4819–4828 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Joulian, C., Ramsing, N. B. & Ingvorsen, K. Congruent phylogenies of most common small-subunit rRNA and dissimilatory sulfite reductase gene sequences retrieved from estuarine sediments. Appl. Environ. Microbiol. 67, 3314–3318 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Kjeldsen, K. U. et al. Diversity of sulfate-reducing bacteria from an extreme hypersaline sediment, Great Salt Lake (Utah). FEMS Microbiol. Ecol. 60, 287–298 (2007).
  Article CAS PubMed Google Scholar
• Leloup, J., Quillet, L., Berthe, T. & Petit, F. Diversity of the dsrAB (dissimilatory sulfite reductase) gene sequences retrieved from two contrasting mudflats of the Seine estuary, France. FEMS Microbiol. Ecol. 55, 230–238 (2006).
  Article CAS PubMed Google Scholar
• Liu, X., Bagwell, C. E., Wu, L., Devol, A. H. & Zhou, J. Molecular diversity of sulfate-reducing bacteria from two different continental margin habitats. Appl. Environ. Microbiol. 69, 6073–6081 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Zhou, J. Microarrays for bacterial detection and microbial community analysis. Curr. Opin. Microbiol. 6, 288–294 (2003).
  Article CAS PubMed Google Scholar
• Brodie, E. L. et al. Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl. Environ. Microbiol. 72, 6288–6298 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• He, Z. et al. GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity. ISME J. 4, 1167–1179 (2010). This article marks the release of an updated GeoChip 3.0, with details for selected gene families, and describes its use to analyse the effects of plant diversity on the functional diversity and structure of soil microbial communities.
  Article CAS PubMed Google Scholar
• Loy, A., Kusel, K., Lehner, A., Drake, H. L. & Wagner, M. Microarray and functional gene analyses of sulfate-reducing prokaryotes in low-sulfate, acidic fens reveal cooccurrence of recognized genera and novel lineages. Appl. Environ. Microbiol. 70, 6998–7009 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Loy, A. et al. Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl. Environ. Microbiol. 68, 5064–5081 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hazen, T. C. et al. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330, 204–208 (2010). This paper details the use of GeoChip 4.0 and other technologies to examine the potential of indigenous microbial communities to degrade contaminants from the oil spill in the Gulf of Mexico.
  Article CAS PubMed Google Scholar
• Van Nostrand, J. D. et al. GeoChip-based analysis of functional microbial communities during the reoxidation of a bioreduced uranium-contaminated aquifer. Environ. Microbiol. 11, 2611–2626 (2009).
  Article CAS PubMed Google Scholar
• Xu, M. et al. Responses of microbial community functional structures to pilot-scale uranium in situ bioremediation. ISME J. 4, 1060–1070 (2010).
  Article PubMed Google Scholar
• Wang, F. et al. GeoChip-based analysis of metabolic diversity of microbial communities at the Juan de Fuca Ridge hydrothermal vent. Proc. Natl Acad. Sci. USA 106, 4840–4845 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Mason, O. U. et al. Prokaryotic diversity, distribution, and insights into their role in biogeochemical cycling in marine basalts. ISME J. 3, 231–242 (2009).
  Article CAS PubMed Google Scholar
• Aitken, C. M., Jones, D. M. & Larter, S. R. Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs. Nature 431, 291–294 (2004).
  Article CAS PubMed Google Scholar
• Head, I. M., Jones, D. M. & Larter, S. R. Biological activity in the deep subsurface and the origin of heavy oil. Nature 426, 344–352 (2003).
  Article CAS PubMed Google Scholar
• Jones, D. M. et al. Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451, 176–180 (2008).
  Article CAS PubMed Google Scholar
• Kniemeyer, O. et al. Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449, 898–901 (2007).
  Article CAS PubMed Google Scholar
• Zhou, J., Kang, S., Schadt, C. W. & Garten, C. T. Spatial scaling of functional gene diversity across various microbial taxa. Proc. Natl Acad. Sci. USA 105, 7768–7773 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Liang, Y. et al. Microarray-based analysis of microbial functional diversity along an oil contamination gradient in oil field. FEMS Microbiol. Ecol. 70, 324–333 (2009).
  Article CAS PubMed Google Scholar
• Liang, Y. et al. Functional gene diversity of soil microbial communities from five oil-contaminated fields in China. ISME J. 5, 403–413 (2011).
  Article PubMed Google Scholar
• Xiong, J. et al. Microbial communities and functional genes associated with soil arsenic contamination and rhizosphere of thearsenic hyper-accumulating plant Pteris vittata L. Appl. Environ. Microbiol. 76, 7277–7284 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Miletto, M. et al. Biogeography of sulfate-reducing prokaryotes in river floodplains. FEMS Microbiol. Ecol. 64, 395–406 (2008).
  Article CAS PubMed Google Scholar
• Rastogi, G. et al. Microbial and mineralogical characterizations of soils collected from the deep biosphere of the former homestake gold mine, South Dakota. Microb. Ecol. 60, 539–550 (2010).
  Article CAS PubMed Google Scholar
• Beyenal, H. et al. Uranium immobilization by sulfate-reducing biofilms. Environ. Sci. Technol. 38, 2067–2074 (2004).
  Article CAS PubMed Google Scholar
• Gu, B. et al. Bioreduction of uranium in a contaminated soil column. Environ. Sci. Technol. 39, 4841–4847 (2005).
  Article CAS PubMed Google Scholar
• Bagwell, C. E., Liu, X., Wu, L. & Zhou, J. Effects of legacy nuclear waste on the compositional diversity and distributions of sulfate-reducing bacteria in a terrestrial subsurface aquifer. FEMS Microbiol. Ecol. 55, 424–431 (2006).
  Article CAS PubMed Google Scholar
• Hwang, C. et al. Changes in bacterial community structure correlate with initial operating conditions of a field-scale denitrifying fluidized bed reactor. Appl. Microbiol. Biotechnol. 71, 748–760 (2006).
  Article CAS PubMed Google Scholar
• Nyman, J. et al. Heterogeneous response to biostimulation for U(VI) reduction in replicated sediment microcosms. Biodegradation 17, 303–316 (2006).
  Article CAS PubMed Google Scholar
• Wu, W. M. et al. Pilot-scale in situ bioremedation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability. Environ. Sci. Technol. 40, 3986–3995 (2006).
  Article CAS PubMed Google Scholar
• Michalsen, M. M. et al. Changes in microbial community composition and geochemistry during uranium and technetium bioimmobilization. Appl. Environ. Microbiol. 73, 5885–5896 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Nyman, J., Gentile, M. & Criddle, C. Sulfate requirement for the growth of U(VI)-reducing bacteria in an ethanol-fed enrichment. Bioremed. J. 11, 21–32 (2007).
  Article CAS Google Scholar
• Nyman, J. L., Wu, H. I., Gentile, M. E., Kitanidis, P. K. & Criddle, C. S. Inhibition of a U(VI)- and sulfate-reducing consortia by U(VI). Environ. Sci. Technol. 41, 6528–6533 (2007).
  Article CAS PubMed Google Scholar
• Wu, W. M. et al. In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ. Sci. Technol. 41, 5716–5723 (2007).
  Article CAS PubMed Google Scholar
• Akob, D. M. et al. Functional diversity and electron donor dependence of microbial populations capable of U(VI) reduction in radionuclide-contaminated subsurface sediments. Appl. Environ. Microbiol. 74, 3159–3170 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Boonchayaanant, B., Kitanidis, P. K. & Criddle, C. S. Growth and cometabolic reduction kinetics of a uranium- and sulfate-reducing Desulfovibrio/Clostridia mixed culture: temperature effects. Biotechnol. Bioeng. 99, 1107–1119 (2008).
  Article CAS PubMed Google Scholar
• Hwang, C. et al. Bacterial community succession during in situ uranium bioremediation: spatial similarities along controlled flow paths. ISME J. 3, 47–64 (2009).
  Article CAS PubMed Google Scholar
• Waldron, P. J. et al. Functional gene array-based analysis of microbial community structure in groundwaters with a gradient of contaminant levels. Environ. Sci. Technol. 43, 3529–3534 (2009).
  Article CAS PubMed Google Scholar
• Boonchayaanant, B., Gu, B., Wang, W., Ortiz, M. & Criddle, C. Can microbially-generated hydrogen sulfide account for the rates of U(VI) reduction by a sulfate-reducing bacterium? Biodegradation 21, 81–95 (2010).
  Article CAS PubMed Google Scholar
• Marcy, Y. et al. Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc. Natl Acad. Sci. USA 104, 11889–11894 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Podar, M. et al. Targeted access to the genomes of low-abundance organisms in complex microbial communities. Appl. Environ. Microbiol. 73, 3205–3214 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Zhou, J., Thompson, D. K., Xu, Y. & Tiedje, J. M. (eds) Microbial Functional Genomics (Wiley & Sons, 2004).
  Book Google Scholar
• Zhou, J. Predictive microbial ecology. Microb. Biotechnol. 2, 154–156 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Kitano, H. Systems biology: a brief overview. Science 295, 1662–1664 (2002).
  Article CAS PubMed Google Scholar
• Gaucher, S. P., Redding, A. M., Mukhopadhyay, A., Keasling, J. D. & Singh, A. K. Post-translational modifications of Desulfovibrio vulgaris Hildenborough sulfate reduction pathway proteins. J. Proteome Res. 7, 2320–2331 (2008).
  Article CAS PubMed Google Scholar
• Han, B. G. et al. Survey of large protein complexes in D. vulgaris reveals great structural diversity. Proc. Natl Acad. Sci. USA 106, 16580–16585 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Tang, Y. et al. Pathway confirmation and flux analysis of central metabolic pathways in Desulfovibrio vulgaris Hildenborough using gas chromatography-mass spectrometry and fourier transform-ion cyclotron resonance mass spectrometry. J. Bacteriol. 189, 940–949 (2007).
  Article CAS PubMed Google Scholar
• Zhou, J. et al. Functional molecular ecological networks. mBio. 1, e00169–e00110 (2010).
  PubMed PubMed Central Google Scholar
• Venceslau, S. S., Lino, R. R. et al. The Qrc membrane complex, related to the alternative complex III, is a menaquinone reductase involved in sulfate respiration. J. Biol. Chem. 285, 22774–22783(2010).
  Article CAS PubMed PubMed Central Google Scholar
• Rosenzweig, R. F., Sharp, R. R., Treves, D. S. & Adams, J. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137, 903–917 (1994).
  CAS PubMed PubMed Central Google Scholar
• Marx, C. J. Getting in touch with your friends. Science 324, 1150–1151 (2009).
  Article CAS PubMed Google Scholar
• Schink, B. Synergistic interactions in the microbial world. Antie van Leeuwenhoek 81, 257–261 (2002).
  Article CAS Google Scholar
• Summers, Z. M. et al. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330, 1413–1415 (2010).
  Article CAS PubMed Google Scholar
• Wu, M. & Eisen, J. A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 9, R151 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599 (2007).
  Article CAS PubMed Google Scholar