Abstract
We investigated the diversity and activity of sulfate-reducing prokaryotes (SRP) in a 3.5-m sediment core taken from a heavy metal-contaminated site in the Medway Estuary, UK. The abundance of SRPs was quantified by qPCR of the dissimilatory sulfite reductase gene β-subunit (dsrB) and taking into account DNA extraction efficiency. This showed that SRPs were abundant throughout the core with maximum values in the top 50 cm of the sediment core making up 22.4% of the total bacterial community and were 13.6% at 250 cm deep. Gene libraries for dsrA (dissimilatory sulfite reductase α-subunit) were constructed from the heavily contaminated (heavy metals) surface sediment (top 20 cm) and from the less contaminated and sulfate-depleted, deeper zone (250 cm). Certain cloned sequences were similar to dsrA found in members of the Syntrophobacteraceae, Desulfobacteraceae and Desulfovibrionaceae as well as a large fraction (60%) of novel sequences that formed a deep branching dsrA lineage. Phylogenetic analysis of metabolically active SRPs was performed by reverse transcription PCR and single strand conformational polymorphism analysis (RT-PCR–SSCP) of dsrA genes derived from extracted sediment RNA. Subsequent comparative sequence analysis of excised SSCP bands revealed a high transcriptional activity of dsrA belonging to Desulfovibrio species in the surface sediment. These results may suggest that members of the Desulfovibrionaceae are more active than other SRP groups in heavy metal-contaminated surface sediments.
Similar content being viewed by others
References
Agrawal A, Lal B (2009) Rapid detection and quantification of bisulfite reductase genes in oil field samples using real-time PCR. FEMS Micobiol Ecol 69:301–312
Alazard D, Dukan S, Urios A, Verhé F, Bouabida N, Morel F, Thomas P, Garcia JL, Ollivier B (2003) Desulfovibrio hydrothermalis sp. nov., a novel sulfate-reducing bacterium isolated from hydrothermal vents. Int J Syst Evol Micr 53:173–178
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Amann R, Fuchs B (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat Rev Microbiol 6:339–348
Bagwell CE, Liu X, Wu L, Zhou J (2006) 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
Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83
Billon G, Ouddane B, Boughriet A (2001) Chemical speciation of sulfur compounds in surface sediments from three bays (Fresnaye, Seine and Authie) in northern France, and identification of some factors controlling their generation. Talanta 53:971–981
Boyle AW, Phelps CD, Young LY (1999) Isolation from estuarine sediments of a Desulfovibrio strain which can grow on lactate coupled to the reductive dehalogenation of 2, 4, 6-tribromophenol. Appl Environ Microbiol 65:1133–1140
Brown SD, Gilmour CC, Kucken AM, Wall JD, Elias DA, Podar M, Chertkov O, Held B, Bruce DC, Detter JC, Tapia R, Han CS, Lynne A, Goodwin LA, Cheng JF, Pitluck S, Woyke T, Mikhailova N, Ivanova NN, Han J, Lucas S, Lapidus AL, Land ML, Hauser LR, Palumbo AV (2011) Genome sequence of mercury-methylating Desulfovibrio desulfuricans ND132. J Bacteriol. doi:10.1128, in press
Burgmann H, Pesaro M, Widmer F, Zeyer J (2001) A strategy for optimizing quality and quantity of DNA extracted from soil. J Microbiol Methods 45:7–20
Cabrera G, Perez R, Gomez JM, Abalos A, Cantero D (2006) Toxic effects of dissolved heavy metals on Desulfovibrio vulgaris and Desulfovibrio sp. strains. J Hazard Mater 135:40–46
Castro H, Reddy KR, Ogram A (2002) Composition and function of sulfate-reducing Prokaryotes in eutrophic and pristine areas of the Florida everglades. Appl Environ Microbiol 68:6129–6137
Chin KJ, Sharma ML, Russell LA, O' Neill KR, Lovley DR (2008) Quantifying expression of a dissimilatory (bi) sulfite reductase gene in petroleum-contaminated marine harbour sediments. Microbiol Ecol 55:489–499
Cundy AB, Hopkinson L, Lafite R, Spencer K, Taylor JA, Ouddane B, Heppell CM, Carey PJ, Charman R, Shell D (2005) Heavy metal distribution and accumulation in two Spartina sp.-dominated macrotidal salt marshes from the Seine estuary (France) and the Medway estuary (UK). Appl Geochem 20:1195–1208
Cundy AB, Lafite R, Taylor JA, Hopkinson L, Deloffre J, Charman R, Gilpin M, Spencer KL, Carey PJ, Heppell CM (2007) Sediment transfer and accumulation in two contrasting salt marsh/mudflat systems: the Seine estuary (France) and the Medway estuary (UK). Hydrobiologia 588:125–134
Cypionka H (2000) Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54:827–848
Daims H, Lücker S, Wagner M (2005) Daime, a novel image analysis program for microbial ecology and biofilm research. Environ Microbiol 8:200–213
Dar SA, Yao L, van Dongen U, Kuenen JG, Muyzer G (2007) Analysis of diversity and activity of sulfate-reducing bacterial communities in sulfidogenic bioreactors using 16S rRNA and dsrB genes as molecular markers. Appl Environ Microbiol 73:594–604
De Lipthay JR, Enzinger C, Johnsen K, Aamand J, Sorensen SJ (2004) Impact of DNA extraction method on bacterial community composition measured by denaturing gradient gel electrophoresis. Soil Biol Biochem 36:1607–1614
Deloffre J, Verney R, Lafite R, Lesueur P, Lesourd S, Cundy AB (2007) Sedimentation on intertidal mudflats in the lower part of macrotidal estuaries: sedimentation rhythms and their preservation. Mar Geol 241:19–32
Dhillon A, Teske A, Dillon J, Stahl DA, Sogin ML (2003) Molecular characterization of sulfate-reducing bacteria in the Guaymas Basin. Appl Environ Microbiol 69:2765–2772
Duran R, Ranchou-Peyruse M, Menuet V, Monperrus M, Bareille G, Goni MS, Salvado JC, Amouroux D, Guyoneaud R, Donard OFX, Caumette P (2008) Mercury methylation by a microbial community from sediments of the Adour Estuary (Bay of Biscay, France). Environ Pollut 156:951–958
Edmonds JW, Weston NB, Joye SB, Moran MA (2008) Variation in prokaryotic community composition as a function of resource availability in tidal creek sediments. Appl Environ Microbiol 74:1836–1844
Ellis RJ, Morgan P, Weightman AD, Fry JC (2003) Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl Environ Microbiol 69:3223–3230
ETWB (2002) Environment, transport and work bureau technical circular. Management of dredged/excavated sediment No. 34. Government Printer, Hong Kong
Foti M, Sorokin DY, Lomans B, Mussman M, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G (2007) Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl Environ Microbiol 73:2093–2100
Fournier M, Aubert C, Dermoun Z, Durand MC, Moinier D, Dolla A (2006) Response of the anaerobe Desulfovibrio vulgaris Hildenborough to oxidative conditions: proteome and transcript analysis. Biochimie 88:85–94
Geets J, Borremans B, Diels L, Springael D, Vangronsveld J, Van Der Lelie D, Vanbroekhoven K (2006) DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria. J Microbiol Methods 66:194–205
Gihring TM, Zhang G, Brandt CC, Brooks SC, Campbell JH, Carroll S, Criddle CS, Green SJ, Jardine P, Kostka JE, Lowe K, Mehlhorn TL, Overholt W, Watson DB, Yang Z, Wu WM, Schadt CW (2011) A limited microbial consortium is responsible for extended bioreduction of uranium in a contaminated aquifer. AEM Accepts, published online ahead of print on 15 July 2011
Gillan DC, Danis B, Pernet P, Joly G, Dubois P (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Appl Env Microbiol 71:679–690
Gittel A, Mußmann M, Sass H, Cypionka H, Knneke M (2008) Identity and abundance of active sulfate-reducing bacteria in deep tidal flat sediments determined by directed cultivation and CARD-FISH analysis. Environ Microbiol 10:2645–2658
Glavac D, Dean M (1993) Optimization of the single-strand conformation polymorphism (SSCP) technique for detection of point mutations. Hum Mutat 2:404–414
Gotelli NJ, Entsminger GL (2006) EcoSim: null models software for ecology. Version 7.0. Acquired Intelligence Inc., Kesey-Bear. http://www.garyentsminger.com/ecosim/ecosim.htm
Hadas O, Pinkas R, Malinszy-Rushansky N, Markel D, Lazar B (2001) Sulfate reduction in Lake Agmon, Israel. Sci Total Environ 266:203–209
Haouari O, Fardeau ML, Casalot L, Tholozan JL, Hamdi M, Ollivier B (2006) Isolation of sulfate-reducing bacteria from Tunisian marine sediments and description of Desulfovibrio bizertensis sp. nov. Int J Syst Evol Micr 56:2909–2913
Harrison BK, Zhang H, Berelson W, Orphan VJ (2009) Variations in archaeal and bacterial diversity associated with the sulfate–methane transition zone in continental margin sediments (Santa Barbara Basin, California). Appl Environ Microbiol 75:1487–1499
He J, Xu Z, Hughes J (2005) Pre-lysis washing improves DNA extraction from a forest soil. Soil Biol Biochem 37:2337–2341
Herrmann S, Kleinsteuber S, Neu TR, Richnow HH, Vogt C (2008) Enrichment of anaerobic benzene-degrading microorganisms by in situ microcosms. FEMS Microbiol Ecol 63:94–106
Jiang W, Fan W (2008) Bioremediation of heavy metal-contaminated soils by sulfate-reducing bacteria. Ann NY Acad Sci 1140:446–454
Jiang L, Zheng Y, Peng X, Zhou H, Zhang C, Xiao X, Wang F (2009) Vertical distribution and diversity of sulfate-reducing prokaryotes in the Pearl River estuarine sediments, Southern China. FEMS Microbiol Ecol 70:249–262
Jin S, Fallgren PH, Bilgin AA, Morris JM, Barnes PW (2007) Bioremediation of benzene, ethylbenzene, and xylenes in groundwater under iron-amended, sulfate-reducing conditions. Environ Toxicol Chem 26:249–253
Jørgensen BB (1982) Mineralization of organic matter in the sea bed—the role of sulfate reduction. Nature 296:443–645
Jørgensen, B B, Nelson, D C (2004) Sulfide oxidation in marine sediments: geochemistry meets microbiology. In “Sulfur biogeochemistry—past and present” Publisher Geological Society of America 63–81
Joulian C, Ramsing NB, Ingvorsen K (2001) Congruent phylogenies of most common small-subunit rRNA and dissimilatory sulfite reductase gene sequences retrieved from estuarine sediments. Appl Environ Microbiol 67:3314–3318
Kaneko R, Hayashi T, Tanahashi M, Naganuma T (2007) Phylogenetic diversity and distribution of dissimilatory sulfite reductase genes from deep-sea sediment cores. Mar Biotech 9:429–436
Kawahara N, Shigematsu K, Miura S, Miyadai T, Kondo R (2008) Distribution of sulfate-reducing bacteria in fish farm sediments on the coast of southern Fukui Prefecture, Japan. Plankton Benth Res 3:42–45
Kjeldsen KU, Tang L, Jorrgensen MG, Ingvorsen K (2009) Enumeration and identification of dominant types of sulfate-reducing bacteria in pulp from a paper recycling plant: a multiphasic approach. FEMS Microbiol Ecol 69:481–494
Klappenbach JL, Saxman PH, Cole JR, Schmidt TM (2001) rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res 29:181–184
Klein M, Friedrich M, Roger AJ, Hugenholtz P, Fishbain S, Abicht H, Blackall LL, Stahl DA, Wagner M (2001) Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J Bacteriol 183:6028–6035
Kondo R, Nedwell D, Purdy K, Silva S (2004) Detection and enumeration of sulfate-reducing bacteria in estuarine sediments by competitive PCR. Geomicrobiol J 21:145–157
Kondo R, Purdy KJ, Silva SQ, Nedwell DB (2007) Spatial dynamics of sulfate-reducing bacterial compositions in sediment along a salinity gradient in a UK estuary. Microbes Environ 22:11–19
Kowalchuk GA, Stephen JR, De Boer W, Prosser JI, Embley TM, Woldendorp JW (1997) Analysis of ammoniaoxidizing bacteria of the beta subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16S ribosomal DNA fragments. Appl Environ Microbiol 63:1489–1497
Kristensen E, Bodenbender J, Jensen MH, Rennenberg H, Jensen KM (2000) Sulfur cycling of intertidal Wadden Sea sediments (Konigshafen, Island of Sylt, Germany): sulfate reduction and sulfur gas emission. J Sea Res 43:93–104
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Labrenz M, Druschel GK, Thomsen-Ebert T, Gilbert B, Welch SA, Kemner KM, Logan GA, Summons RE, Stasio GD, Bond PL (2000) Formation of sphalerite (ZnS) deposits in natural biofilms of sulfate-reducing bacteria. Science 290:1744–1747
Lehours AC, Bardot C, Thenot A, Debroas D, Fonty G (2005) Anaerobic microbial communities in lake Pavin: a unique meromictic lake in France. Appl Environ Microbiol 71:7389–7400
Leloup J, Quillet L, Oger C, Boust D, Petit F (2004) Molecular quantification of sulfate-reducing procaryotes (carrying dsrAB genes) by competitive PCR in estuarine sediments. FEMS Microbiol Ecol 47:207–214
Leloup J, Petit F, Boust D, Deloffre J, Bally G, Clarisse O, Quillet L (2005) Dynamics of sulfate-reducing procaryotes (dsrAB genes) in two contrasting mudflats of the Seine estuary (France). Microbiol Ecol 50:307–314
Leloup J, Quillet L, Berthe T, Petit F (2006) 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
Leloup J, Loy A, Knab NJ, Borowski C, Wagner M, Jørgensen BB (2007) Diversity and abundance of sulfate-reducing procaryotes in the sulfate and methane zones of a marine sediment, Black Sea. Environ Microbiol 9:131–142
Leloup J, Fossing H, Kohls K, Holmkvist L, Borowski C, Jørgensen BB (2009) Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation. Environ Microbiol 11:1278–1291
Liu XZ, Zhang LM, Prosser JI, He JZ (2009) Abundance and community structure of sulfate reducing prokaryotes in a paddy soil of southern China under different fertilization regimes. Soil Biol Biochem 41:687–694
Llobet-Brossa E, Rosselo-Mora R, Amann R (1998) Microbial community composition of Wadden Sea sediments as revealed by fluorescence in situ hybridization. Appl Environ Microbiol 64:2691–2696
Lloyd JR, Mabbett AN, Williams DR, Macaskie LE (2001) Metal reduction by sulphate-reducing bacteria: physiological diversity and metal specificity. Hydrometall 59:327–337
Lloyd KG, MacGregor BJ, Teske A (2010a) Quantitative PCR methods for RNA and DNA in marine sediments: maximizing yield while overcoming inhibition. FEMS Microbiol Ecol 72:143–151
Lloyd KG, Albert DB, Biddle JF, Chanton JP, Pizarro O, Andreas Teske (2010b) Spatial structure and activity of sedimentary microbial communities underlying a Beggiatoa spp. mat in a Gulf of Mexico hydrocarbon seep. PLoS One 5:e8738
Lofi J, Weber O (2001) SCOPIX-digital processing of x-ray images for the enhancement of sedimentary structures in undisturbed core slabs. Geol-Mar Lett 20:182–186
Lücker S, Steger D, Kjeldsen KU, MacGregor BJ, Wagner M, Loy A (2007) Improved 16S rRNA-targeted probe set for analysis of sulfate-reducing bacteria by fluorescence in situ hybridization. J Microbiol Methods 69:523–528
Luna GM, Manini E, Danovaro R (2002) Large fraction of dead and inactive bacteria in coastal marine sediments: comparison of protocols for determination and ecological significance. Appl Environ Microbiol 68:3509–3513
Luna GM, Dell'Anno A, Danovaro R (2006) DNA extraction procedure: a critical issue for bacterial diversity assessment in marine sediments. Environ Microbiol 8:308–320
Luo Q, Groh JL, Ballard JD, Krumholz LR (2007) Identification of genes that confer sediment fitness to Desulfovibrio desulfuricans G20. Appl Environ Microbiol 73:6305–6312
Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799
Mc Inerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM, Schink B, Rohlin L, Gunsalus RP (2008) Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann NY Acad Sci 1125:58–72
Migeon S, Weber O, Faugeres JC, Saint-Paul J (1999) SCOPIX: a new x-ray imaging system for core analysis. Geol Mar Lett 18:251–255
Miskin IP, Farrimond P, Head IM (1999) Identification of novel bacterial lineages as active members of microbial populations in a freshwater sediment using rapid RNA extraction procedure and RT-PCR. Microbiology 145:1977–1987
Miyatake T, MacGregor BJ, Boschker HTS (2009) Linking microbial community function to phylogeny of sulfate-reducing Deltaproteobacteria in marine sediments by combining stable isotope probing with magnetic-bead capture hybridization of 16S rRNA. Appl Environ Microbiol 75:4927–4935
Moreau JW, Zierenberg RA, Banfield JF (2010) Diversity of dissimilatory sulfite reductase genes (dsrAB) in a salt marsh impacted by long-term acid mine drainage. Appl Environ Microbiol 76:4819–4828
Mumy KL, Findlay RH (2004) Convenient determination of DNA extraction efficiency using an external DNA recovery standard and quantitative–competitive PCR. J Microbiol Methods 57:259–268
Mußmann M, Ishii K, Rabus R, Amann R (2005) Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mudflat of the Wadden Sea. Environ Microbiol 7:405–418
Muyzer G, De Wall EC, Uitierlinden AG (1993) Gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Naz N, Young HK, Ahmed N, Gadd GM (2005) Cadmium accumulation and DNA homology with metal resistance genes in sulfate-reducing bacteria. Appl Environ Microb 71:4610–4618
Oger C, Berthe T, Quillet L, Barray S, Chiffoleau JF, Petit F (2001) Estimation of the abundance of the cadmium resistance gene cadA in microbial communities in polluted estuary water. Res Microbiol 152:671–678
Orphan VJ, Turk KA, Green AM, House CH (2009) Patterns of 15 N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environ Microbiol 11:1777–1791
Ouddane B, Mikac N, Cundy AB, Quillet L, Fischer JC (2008) A comparative study of mercury distribution and methylation in mudflats from two macrotidal estuaries: the Seine (France) and the Medway (United Kingdom). Appl Geochem 23:618–631
Pavissich JP, Silva M, Gonzalez B (2010) Sulfate reduction, molecular diversity, and copper amendment effects in bacterial communities enriched from sediments exposed to copper mining residues. Environ Toxicol Chem 29:256–264
Perez-Jimenez JR, Kerkhof LJ (2005) Phylogeography of sulfate reducing bacteria among disturbed sediments, disclosed by analysis of the dissimilatory sulfite reductase genes (dsrAB). Appl Environ Microbiol 71:1004–1011
Perez-Jimenez JR, Young LY, Kerkhof LJ (2001) Molecular characterization of sulfate-reducing bacteria in anaerobic hydrocarbon-degrading consortia and pure cultures using the dissimilatory sulfite reductase (dsrAB) genes. FEMS Microbiol Ecol 35:145–150
Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ (2008) Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci USA 105:7052–7057
Plugge CM, Scholten JCM, Culley DE, Nie L, Brockman FJ, Zhang W (2010) Global transcriptomics analysis of the Desulfovibrio vulgaris change from syntrophic growth with Methanosarcina barkeri to sulfidogenic metabolism. Microbiology 156:2746–2756
Rabus R, Hansen TA, Widdel F (2006) Dissimilatory sulfate- and sulfur-reducing prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes, 3rd edition: an evolving electronic resource for the microbiological community, vol 2. Springer, New York, pp 659–768
Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394
Robador A, Brachert V, Jorgensen BB (2009) The impact of temperature change on the activity and community composition of sulfate-reducing bacteria in arctic versus temperate marine sediments. Environ Microbiol 11:1692–1703
Roose-Amsaleg CL, Garnier-Sillam E, Harry M (2001) Extraction and purification of microbial DNA from soil and sediment samples. Appl Soil Ecol 18:47–60
Rose P, Harkin JM, Hickey WJ (2003) Competitive touchdown PCR for estimation of Escherichia coli DNA recovery in soil DNA extraction. J Microbiol Methods 52:29–38
Sagova-Mareckova M, Cermak L, Novotna J, Plhackova K, Forstova J, Kopecky J (2008) Innovative methods for soil DNA purification tested in soils with widely differing characteristics. Appl Environ Microbiol 74:2902–2907
Sahm K, Knoblauch C, Amann R (1999) Phylogenetic affiliation and quantification of psychrophilic sulfate-reducing isolates in marine arctic sediments. Appl Environ Microbiol 65:3976
Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sass H, Berchtold M, Branke J, König H, Cypionka H, Babenzien HD (1998) Psychrotolerant sulfate-reducing bacteria from an oxic freshwater sediment, description of Desulfovibrio cuneatus sp. nov. and Desulfovibrio litoralis sp. nov. Syst Appl Microbiol 21:212–219
Schippers A, Neretin LN (2006) Quantification of microbial communities in near-surface and deeply buried marine sediments on the Peru continental margin using real-time PCR. Environ Microbiol 8:1251–1260
Scholten JC, Culley DE, Brockman FJ, Gang Wu G, Zhang W (2007) Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer. Biochem Biophys Res Com 352:48–54
Shao D, Liang P, Kang Y, Wanga H, Cheng Z, Wua S, Shi J, Chun Lap Lo S, Wangd W, Wong MH (2011) Mercury species of sediment and fish in freshwater fish ponds around the Pearl River Delta, PR China: human health risk assessment. Chemosphere. doi:10.1016, in press
Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16SrRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4373–4376
Stevens H, Brinkhoff T, Rink B, Vollmers J, Simon M (2007) Diversity and abundance of Gram positive bacteria in a tidal flat ecosystem. Environ Microbiol 9:1810–1822
Suzuki D, Ueki A, Amaishi A, Ueki K (2007) Desulfobulbus japonicus sp. nov., a novel Gram-negative propionate-oxidizing, sulfate-reducing bacterium isolated from an estuarine sediment in Japan. Int J Syst Evol Micr 57:849–855
Tebo BM, Obraztsova AY (1998) Sulfate-reducing bacterium grows with Cr (VI), U (VI), Mn (IV), and Fe (III) as electron acceptors. FEMS Microbiol Lett 162:193–198
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Thomsen TR, Finster K, Ramsing NB (2001) Biogeochemical and molecular signatures of anaerobic methane oxidation in a marine sediment. Appl Environ Microbiol 67:1646–1656
Tsai YL, Olson BH (1991) Rapid method for direct extraction of DNA from soil and sediments. Appl Environ Microbiol 57:1070–1074
Tujula NA, Holmström C, Mußmann M, Amann R, Kjelleberg S, Crocetti GR (2006) A CARD–FISH protocol for the identification and enumeration of epiphytic bacteria on marine algae. J Microbiol Methods 65:604–607
Utgikar VP, Harmon SM, Chaudhary N, Tabak HH, Govind R, Haines JR (2002) Inhibition of sulfate-reducing bacteria by metal sulfide formation in bioremediation of acid mine drainage. Environ Toxicol 17:40–48
Utgikar VP, Tabak HH, Haines JR, Govind R (2003) Quantification of toxic and inhibitory impact of copper and zinc on mixed cultures of sulfate-reducing bacteria. Biotechnol Bioeng 82:306–312
Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338
Vandieken V, Knoblauch C, Jorgensen BB (2006) Desulfovibrio frigidus sp. nov. and Desulfovibrio ferrireducens sp. nov., psychrotolerant bacteria isolated from Arctic fjord sediments (Svalbard) with the ability to reduce Fe (III). Int J Syst Evol Micr 56:681–685
Villanueva L, Haveman SA, Summers ZM, Lovley DR (2008) Quantification of Desulfovibrio vulgaris dissimilatory sulfite reductase gene expression during electron donor- and electron acceptor-limited growth. Appl Environ Microbiol 74:5850–5853
Voordouw G, Walker JE, Brenner S (1985) Cloning of the gene encoding the hydrogenase from Desulfovibrio vulgaris (Hildenborough) and determination of the NH2-terminal sequence. Eur J Biochem 148:509–514
Wagner M, Roger AJ, Flax JL, Brusseau GA, Stahl DA (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J Bacteriol 180:2975–2982
Wawer C, Jetten MSM, Muyzer G (1997) Genetic diversity and expression of the [NiFe] Hydrogenase large-subunit gene of Desulfovibrio spp. in environmental samples. Appl Environ Microbiol 63:4360–4369
Webb JS, McGinness S, Lappin-Scott HM (1998) Metal removal by sulfate-reducing bacteria from natural and constructed wetlands. J Appl Microbiol 84:240–248
Webster G, Watt LC, Rinna J, Fry JC, Evershed RP, Parkes RJ, Weightman AJ (2006) A comparison of stable-isotope probing of DNA and phospholipid fatty acids to study prokaryotic functional diversity in sulfate-reducing marine sediment enrichment slurries. Environ Microbiol 9:1575–1589
Wilms R, Sass H, Köpke B, Cypionka H, Engelen B (2007) Methane and sulfate profiles within the subsurface of a tidal flat are reflected by the distribution of sulfate-reducing bacteria and methanogenic archaea. FEMS Microbiol Ecol 59:611–621
Woebken D, Fuchs BM, Kuypers MM, Amann R (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73:4648–4657
Zhang W, Ki JS, Qian PY (2008) Microbial diversity in polluted harbor sediments I: bacterial community assessment based on four clone libraries of 16S rDNA. Estuarine Coastal Shelf Sci 76:668–681
Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microb 62:316–322
Acknowledgements
This work was supported by the European Union INTERREG IIIa program RIMEW (Rives-Manche Estuarine Watch). We thank Dilys Moscato and Vic Norris for help with the English.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Quillet, L., Besaury, L., Popova, M. et al. Abundance, Diversity and Activity of Sulfate-Reducing Prokaryotes in Heavy Metal-Contaminated Sediment from a Salt Marsh in the Medway Estuary (UK). Mar Biotechnol 14, 363–381 (2012). https://doi.org/10.1007/s10126-011-9420-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-011-9420-5