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Assessing the Diversity of Benthic Sulfate-Reducing Microorganisms in Northwestern Gulf of Mexico by Illumina Sequencing of dsrB Gene

  • Environmental Microbiology
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Abstract

This study investigates the community composition, structure, and abundance of sulfate-reducing microorganisms (SRM) in surficial sediments of the Northwestern Gulf of Mexico (NWGoM) along a bathymetric gradient. For these purposes, Illumina sequencing and quantitative PCR (qPCR) of the dissimilatory sulfite reductase gene beta subunit (dsrB gene) were performed. Bioinformatic analyses indicated that SRM community was predominantly composed by members of Proteobacteria and Firmicutes across all the samples. However, Actinobacteria, Thermodesulfobacteria, and Chlorobi were also detected. Phylogenetic analysis indicated that unassigned dsrB sequences were related to Deltaproteobacteria and Nitrospirota superclusters, Euryarchaeota, and to environmental clusters. PCoA ordination revealed that samples clustered in three different groups. PERMANOVA indicated that water depth, temperature, redox, and nickel and cadmium content were the main environmental drivers for the SRM communities in the studied sites. Alpha diversity and abundance of SRM were lower for deeper sites, suggesting decreasing sulfate reduction activity with respect to water depth. This study contributes with the understanding of distribution and composition of dsrAB-containing microorganisms involved in sulfur transformations that may contribute to the resilience and stability of the benthic microbial communities facing metal and hydrocarbon pollution in the NWGoM, a region of recent development for oil and gas drilling.

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References

  1. Pallud C, Van Cappellen P (2006) Kinetics of microbial sulfate reduction in estuarine sediments. Geochim Cosmochim Acta 70:1148–1162. https://doi.org/10.1016/j.gca.2005.11.002

    Article  CAS  Google Scholar 

  2. Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nature 6:441–454. https://doi.org/10.1038/nrmicro1892

    Article  CAS  Google Scholar 

  3. Labrenz M, Druschel GK, Thomsen-Ebert T et al (2000) Formation of spharellite (ZnS) deposits in natural biofilms of sulfate-reducing bacteria. Science (80- ) 290:1744–1747. https://doi.org/10.1126/science.290.5497.1744

    Article  CAS  Google Scholar 

  4. Jørgensen BB (1982) Mineralization of organic matter in the seabed - the role of sulfate reduction. Nature 296:643–645. https://doi.org/10.1038/296643a0

    Article  Google Scholar 

  5. Jørgensen BB, Findlay AJ, Pellerin A (2019) The biogeochemical sulfur cycle of marine sediments. Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.00849

  6. Rabus R, Venceslau SS, Wöhlbrand L et al (2015) A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes. Adv. Microb. Physiol, pp 55–321. https://doi.org/10.1016/bs.ampbs.2015.05.002

    Chapter  Google Scholar 

  7. Müller AL, Kjeldsen KU, Rattei T, Pester M, Loy A (2015) Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi) sulfite reductases. ISME J 9:1152–1165. https://doi.org/10.1038/ismej.2014.208

    Article  CAS  PubMed  Google Scholar 

  8. Anantharaman K, Hausmann B, Jungbluth SP, Kantor RS, Lavy A, Warren LA, Rappé MS, Pester M, Loy A, Thomas BC, Banfield JF (2018) Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle. ISME J 12:1715–1728. https://doi.org/10.1038/s41396-018-0078-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Colman DR, Lindsay MR, Amenabar MJ, Fernandes-Martins MC, Roden ER, Boyd ES (2020) Phylogenomic analysis of novel Diaforarchaea is consistent with sulfite but not sulfate reduction in volcanic environments on early Earth. ISME J 14:1316–1331. https://doi.org/10.1038/s41396-020-0611-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Vuillemin A, Kerrigan Z, D’Hondt S, Orsi WD (2020) Chloroflexi persisting for millions of years in oxic and anoxic deep-sea clay. bioRxiv:2020.05.26.116590. https://doi.org/10.1101/2020.05.26.116590

  11. Plugge CM, Zhang W, Scholten JCM, Stams AJM (2011) Metabolic flexibility of sulfate-reducing bacteria. Front Microbiol 2:1–8. https://doi.org/10.3389/fmicb.2011.00081

    Article  CAS  Google Scholar 

  12. Wagner M, Loy A, Klein M et al (2005) Functional marker genes for identification of sulfate-reducing prokaryotes. Methods Enzymol, pp 469–489. https://doi.org/10.1016/S0076-6879(05)97029-8

    Chapter  Google Scholar 

  13. 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. https://doi.org/10.1016/j.mimet.2007.02.009

    Article  CAS  PubMed  Google Scholar 

  14. Larsen Ø, Lien T, Birkeland N-K (2001) A novel organization of the dissimilatory sulfite reductase operon of Thermodesulforhabdus norvegica verified by RT-PCR. FEMS Microbiol Lett 203:81–85. https://doi.org/10.1111/j.1574-6968.2001.tb10824.x

    Article  CAS  PubMed  Google Scholar 

  15. 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. https://doi.org/10.1128/JB.183.20.6028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jochum LM, Schreiber L, Marshall IPG, Jørgensen BB, Schramm A, Kjeldsen KU (2018) Single-cell genomics reveals a diverse metabolic potential of uncultivated Desulfatiglans-related deltaproteobacteria widely distributed in marine sediment. Front Microbiol 9:1–16. https://doi.org/10.3389/fmicb.2018.02038

    Article  Google Scholar 

  17. Kaneko R, Hayashi T, Tanahashi M, Naganuma T (2007) Phylogenetic diversity and distribution of dissimilatory sulfite reductase genes from deep-sea sediment cores. Mar Biotechnol 9:429–436. https://doi.org/10.1007/s10126-007-9003-7

    Article  CAS  Google Scholar 

  18. Li X-X, Liu J-F, Zhou L, Mbadinga SM, Yang SZ, Gu JD, Mu BZ (2017) Diversity and composition of sulfate-reducing microbial communities based on genomic DNA and RNA transcription in production water of high temperature and corrosive oil reservoir. Front Microbiol 8:1–17. https://doi.org/10.3389/fmicb.2017.01011

    Article  Google Scholar 

  19. Bagwell CE, Formolo M, Ye Q, Yeager CM, Lyons TW, Zhang CL (2009) Direct analysis of sulfate reducing bacterial communities in gas hydrate-impacted marine sediments by PCR-DGGE. J Basic Microbiol 49:87–92. https://doi.org/10.1002/jobm.200800278

    Article  Google Scholar 

  20. Pérez-Jiménez 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. https://doi.org/10.1016/S0168-6496(00)00123-9

    Article  PubMed  Google Scholar 

  21. Watanabe T, Kojima H, Fukui M (2016) Identity of major sulfur-cycle prokaryotes in freshwater lake ecosystems revealed by a comprehensive phylogenetic study of the dissimilatory adenylylsulfate reductase. Sci Rep 6:1–9. https://doi.org/10.1038/srep36262

    Article  CAS  Google Scholar 

  22. Zhang Y, Zhen Y, Tiezhu M et al (2016) Molecular characterization of sulfate-reducing bacteria community in surface sediments from the adjacent area of Changjiang Estuary. Ocean Coast Sea Res 15:107–116. https://doi.org/10.1007/s11802-016-2781-7

    Article  CAS  Google Scholar 

  23. Zhang Y, Wang X, Zhen Y, Mi T, He H, Yu Z (2017) Microbial diversity and community structure of sulfate-reducing and sulfur-oxidizing bacteria in sediment cores from the East China Sea. Front Microbiol 8:1–17. https://doi.org/10.3389/fmicb.2017.02133

    Article  Google Scholar 

  24. Anderson RK, Scalan RS, Parker PL, Behrens EW (1983) Seep oil and gas in Gulf of Mexico slope sediment. Science (80- ) 222:619–621. https://doi.org/10.1126/science.222.4624.619

    Article  CAS  Google Scholar 

  25. Canfield DE (1991) Sulfate reduction in deep-sea sediments. Am J Sci 291:177–188. https://doi.org/10.2475/ajs.291.2.177

    Article  CAS  PubMed  Google Scholar 

  26. Aharon P, Fu B (2000) Microbial sulfate reduction rates and sulphur and oxygen isotope fractionation at oil and gas seeps in deepwater Gulf of Mexico. Geochim Cosmochim Acta 64:233–246. https://doi.org/10.1016/S0016-7037(99)00292-6

    Article  CAS  Google Scholar 

  27. Joye SB, Boetius A, Orcutt BN, Montoya JP, Schulz HN, Erickson MJ, Lugo SK (2004) The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps. Chem Geol 205:219–238. https://doi.org/10.1016/j.chemgeo.2003.12.019

    Article  CAS  Google Scholar 

  28. Lanoil BD, Sassen R, La Duc MT et al (2001) Bacteria and archaea physically associated with Gulf of Mexico gas hydrates. Appl Environ Microbiol 67:5143–5153. https://doi.org/10.1128/AEM.67.11.5143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mills HJ, Martinez RJ, Story S, Sobecky PA (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA- and RNA-derived clone libraries. Appl Environ Microbiol 71:3235–3247. https://doi.org/10.1128/AEM.71.6.3235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Orcutt BN, Joye SB, Kleindienst S, Knittel K, Ramette A, Reitz A, Samarkin V, Treude T, Boetius A (2010) Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments. Deep Sea Res II Top Stud Oceanogr 57:2008–2021. https://doi.org/10.1016/j.dsr2.2010.05.014

    Article  CAS  Google Scholar 

  31. Shin B, Kim M, Zengler K, Chin KJ, Overholt WA, Gieg LM, Konstantinidis KT, Kostka JE (2019) Anaerobic degradation of hexadecane and phenanthrene coupled to sulfate reduction by enriched consortia from northern Gulf of Mexico seafloor sediment. Sci Rep 9:1–13. https://doi.org/10.1038/s41598-018-36567-x

    Article  CAS  Google Scholar 

  32. Yang T, Speare K, Luke M et al (2016) Distinct bacterial communities in surficial seafloor sediments following the 2010 DWH blowout. Front Microbiol 7:1–18. https://doi.org/10.3389/fmicb.2016.01384

    Article  Google Scholar 

  33. Beazley MJ, Martinez RJ, Rajan S, Powell J, Piceno YM, Tom LM, Andersen GL, Hazen TC, van Nostrand JD, Zhou J, Mortazavi B, Sobecky PA (2012) Microbial community analysis of a coastal salt marsh affected by the DWH oil spill. PLoS One 7:e41305. https://doi.org/10.1371/journal.pone.0041305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Nunoura T, Soffientino B, Blazejak A, Kakuta J, Oida H, Schippers A, Takai K (2009) Subseafloor microbial communities associated with rapid turbidite deposition in the Gulf of Mexico continental slope (IODP Expedition 308). FEMS Microbiol Ecol 69:410–424. https://doi.org/10.1111/j.1574-6941.2009.00718.x

    Article  CAS  PubMed  Google Scholar 

  35. Lloyd KG, Albert DB, Biddle JF et al (2010) Spatial structure and activity of sedimentary microbial communities underlying a Beggiatoa spp. mat in a Gulf of Mexico hydrocarbon seep. PLoS One. https://doi.org/10.1371/journal.pone.0008738

  36. Sánchez-Soto Jiménez MF, Cerqueda-García D, Montero-Muñoz JL, Aguirre-Macedo ML, García-Maldonado JQ (2018) Assessment of the bacterial community structure in shallow and deep sediments of the Perdido Fold Belt region in the Gulf of Mexico. PeerJ 6:e5583. https://doi.org/10.7717/peerj.5583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ramírez D, Vega-Alvarado L, Taboada B, Estradas-Romero A, Soto L, Juárez K (2019) Bacterial diversity in surface sediments from the continental shelf and slope of the North West gulf of Mexico and the presence of hydrocarbon degrading bacteria. Mar Pollut Bull 150:110590. https://doi.org/10.1016/j.marpolbul.2019.110590

    Article  CAS  PubMed  Google Scholar 

  38. Walkley A, Black IA (1934) An examination of the Degtjaeff method for determining soil organic matter, and a proposed modification of the chromatic acid titration method. Soil Sci 37:29–38. https://doi.org/10.1097/00010694-193401000-00003

    Article  CAS  Google Scholar 

  39. Wentworth CK (1992) A scale of grade and class terms for clastic sediments. J Geol 30:377–392. https://doi.org/10.1086/622910

    Article  Google Scholar 

  40. Loring DH, Rantala RTT (1992) Manual for the geochemical analyses of marine sediments and suspended particulate matter. Earth Sci Rev 32:235–283. https://doi.org/10.1016/0012-8252(92)90001-A

    Article  CAS  Google Scholar 

  41. Arcega-Cabrera F, Velázquez-Tavera N, Fargher L, Derrien M, Noreña-Barroso E (2014) Fecal sterols, seasonal variability, and probable sources along the ring of cenotes, Yucatan, Mexico. J Contam Hydrol 168:41–49. https://doi.org/10.1016/j.jconhyd.2014.08.007

    Article  CAS  PubMed  Google Scholar 

  42. Pelikan C, Herbold CW, Hausmann B, Müller AL, Pester M, Loy A (2016) Diversity analysis of sulfite- and sulfate-reducing microorganisms by multiplex dsrA and dsrB amplicon sequencing using new primers and mock community-optimized bioinformatics. Environ Microbiol 18:2994–3009. https://doi.org/10.1111/1462-2920.13139

    Article  CAS  PubMed  Google Scholar 

  43. He H, Zhen Y, Mi T, Xu B, Wang G, Zhang Y, Yu Z (2015) Community composition and distribution of sulfate -and sulfite-reducing prokaryotes in sediments from the Changjiang estuary and adjacent East China Sea. Estuar Coast Shelf Sci 165:75–85. https://doi.org/10.1016/j.ecss.2015.09.005

    Article  CAS  Google Scholar 

  44. 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. https://doi.org/10.1016/j.mimet.2005.11.002

    Article  CAS  PubMed  Google Scholar 

  45. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson II MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:848–857. https://doi.org/10.1038/s41587-019-0209-9

    Article  CAS  Google Scholar 

  46. Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Buchfink B, Xie C, Huson DH (2014) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60. https://doi.org/10.1038/nmeth.3176

    Article  CAS  PubMed  Google Scholar 

  48. Huson DH, Beier S, Flade I, Górska A, el-Hadidi M, Mitra S, Ruscheweyh HJ, Tappu R (2016) MEGAN community edition - interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput Biol 12:1–12. https://doi.org/10.1371/journal.pcbi.1004957

    Article  CAS  Google Scholar 

  49. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:1–11. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  Google Scholar 

  50. Oksanen J (2013) Multivariate analysis of ecological communities in R: vegan tutorial. https://doi.org/10.1016/0169-5347(88)90124-3

  51. Wickham H (2010) ggplot2: elegant graphics for data analysis. J Stat Softw 35:1–3. https://doi.org/10.18637/jss.v035.b01

    Article  Google Scholar 

  52. Paulson JN, Stine OC, Corrada H, Pop M (2013) Robust methods for differential abundance analysis in marker gene surveys. Nat Methods 10:1200–1202. https://doi.org/10.1016/j.physbeh.2017.03.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: A versatile open source tool for metagenomics. PeerJ 2016:1–22. https://doi.org/10.7717/peerj.2584

    Article  Google Scholar 

  54. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164

    Article  CAS  PubMed  Google Scholar 

  56. Di D, Posada D, Kozlov AM et al (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291–294. https://doi.org/10.1093/molbev/msz189

    Article  CAS  Google Scholar 

  57. Letunik I, Bork P (2007) Interactive tree of life (iTOL):na online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128. https://doi.org/10.1093/bioinformatics/btl529

    Article  CAS  Google Scholar 

  58. Devereux R, Winfrey MR, Winfrey J, Stahl DA (1996) Depth profile of sulfate-reducing bacterial ribosomal RNA and mercury methylation in an estuarine sediment. FEMS Microbiol Ecol 20:23–31. https://doi.org/10.1016/0168-6496(96)00011-6

    Article  CAS  Google Scholar 

  59. Bale SJ, Goodman K, Rochelle PA et al (1997) Desulfovibrio profundus sp. nov., a novel barophilic sulfate-reducing bacterium from deep sediment layers in the Japan Sea. Int J Syst Bacteriol 47:515–521. https://doi.org/10.1099/00207713-47-2-515

    Article  CAS  PubMed  Google Scholar 

  60. Mills HJ, Hodges C, Wilson K, MacDonald IR, Sobecky PA (2003) Microbial diversity in sediments associated with surface-breaching gas hydrate mounds in the Gulf of Mexico. FEMS Microbiol Ecol 46:39–52. https://doi.org/10.1016/S0168-6496(03)00191-0

    Article  CAS  PubMed  Google Scholar 

  61. Parkes RJ, Dowling NJE, White DC et al (1993) Characterization of sulphate-reducing bacterial populations within marine and estuarine sediments with different rates of sulphate reduction. FEMS Microbiol Ecol 102:235–250. https://doi.org/10.1016/0378-1097(93)90206-H

    Article  CAS  Google Scholar 

  62. Kondo R, Nedwell DB, Purdy KJ, De Queiroz SS (2004) Detection and enumeration of sulphate-reducing bacteria in estuarine sediments by competitive PCR. Geomicrobiol J 21:145–157. https://doi.org/10.1080/01490450490275307

    Article  CAS  Google Scholar 

  63. Isaksen FM, Bak F, Jørgensen BB (1994) Thermophilic sulfate-reducing bacteria in cold marine sediment. FEMS Microbiol Ecol 14:1–8. https://doi.org/10.1111/j.1574-6941.1994.tb00084.x

    Article  CAS  Google Scholar 

  64. Rezende JR, Kjeldsen KU, Hubert CR et al (2013) Dispersal of thermophilic Desulfotomaculum endospores into Baltic Sea sediments over thousands of years. ISME J 7:72–84. https://doi.org/10.1038/ismej.2012.83

    Article  CAS  PubMed  Google Scholar 

  65. Sass H, Cypionka H, Babenzien HD (1997) Vertical distribution of sulfate-reducing bacteria at the oxic-anoxic interface in sediments of the oligotrophic Lake Stechlin. FEMS Microbiol Ecol 22:245–255. https://doi.org/10.1016/S0168-6496(96)00096-7

    Article  CAS  Google Scholar 

  66. Kang S, Van Nostrand JD, Gough HL et al (2013) Functional gene array – based analysis of microbial communities in heavy metals-contaminated lake sediments. FEMS Microbiol Ecol 86:200–214. https://doi.org/10.1111/1574-6941.12152

    Article  CAS  PubMed  Google Scholar 

  67. Tian H, Gao P, Chen Z, Li Y, Li Y, Wang Y, Zhou J, Li G, Ma T (2017) Compositions and abundances of sulfate-reducing and sulfur-oxidizing microorganisms in water-flooded petroleum reservoirs with different temperatures in China. Front Microbiol 8:1–14. https://doi.org/10.3389/fmicb.2017.00143

    Article  Google Scholar 

  68. Devereux R, Delaney M, Widdel F, Stahl DA (1989) Natural relationships among sulfate-reducing Eubacteria. J Bacteriol 171:6689–6695. https://doi.org/10.1128/jb.171.12.6689-6695.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Slobodkin AI, Slobodkina GB (2019) Diversity of sulfur-disproportionating microorganisms. Microbiol (Russian Fed) 88:509–522. https://doi.org/10.1134/S0026261719050138

    Article  CAS  Google Scholar 

  70. Chakraborty A, Ellefson E, Li C, Gittins D, Brooks JM, Bernard BB, Hubert CRJ (2018) Thermophilic endospores associated with migrated thermogenic hydrocarbons in deep Gulf of Mexico marine sediments. ISME J 12:1895–1906. https://doi.org/10.1038/s41396-018-0108-y

    Article  PubMed  PubMed Central  Google Scholar 

  71. Meza-Padilla R, Enriquez C, Liu Y, Appendini CM (2019) Ocean circulation in the western Gulf of Mexico using self - organizing maps. J Geophys Res Ocean 124:1–16. https://doi.org/10.1029/2018JC014377

    Article  Google Scholar 

  72. Sun H, Spring S, Lapidus A, Davenport K, del Rio TG, Tice H, Nolan M, Copeland A, Cheng JF, Lucas S, Tapia R, Goodwin L, Pitluck S, Ivanova N, Pagani I, Mavromatis K, Ovchinnikova G, Pati A, Chen A, Palaniappan K, Hauser L, Chang YJ, Jeffries CD, Detter JC, Han C, Rohde M, Brambilla E, Göker M, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Land M (2010) Complete genome sequence of Desulfarculus baarsii type strain (2st14 T). Stand Genomic Sci 3:276–284. https://doi.org/10.4056/sigs.1243258

    Article  PubMed  PubMed Central  Google Scholar 

  73. Mohn WW, Tiedje JM (1992) Microbial reductive dehalogenation. Microbiol Rev 56:482–507. https://doi.org/10.1128/mmbr.56.3.482-507.1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 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. https://doi.org/10.1111/j.1462-2920.2008.01855.x

    Article  CAS  PubMed  Google Scholar 

  75. Umezawa K, Kojima H, Kato Y, Fukui M (2020) Disproportionation of inorganic sulfur compounds by a novel autotrophic bacterium belonging to Nitrospirota. Syst Appl Microbiol 43:126110. https://doi.org/10.1016/j.syapm.2020.126110

    Article  CAS  PubMed  Google Scholar 

  76. 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. https://doi.org/10.1128/AEM.69.5.2765-2772.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Mori K, Maruyama A, Urabe T, Suzuki KI, Hanada S (2008) Archaeoglobus infectus sp. nov., a novel thermophilic, chemolithoheterotrophic archaeon isolated from a deep-sea rock collected at Suiyo Seamount, Izu-Bonin Arc, western Pacific Ocean. Int J Syst Evol Microbiol 58:810–816. https://doi.org/10.1099/ijs.0.65422-0

    Article  CAS  PubMed  Google Scholar 

  78. Frank KL, Rogers DR, Olins HC, Vidoudez C, Girguis PR (2013) Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents. ISME J 7:1391–1401. https://doi.org/10.1038/ismej.2013.17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Müller AL, De Rezende JR, Hubert CRJ et al (2014) Endospores of thermophilic bacteria as tracers of microbial dispersal by ocean currents. ISME J 8:1153–1165. https://doi.org/10.1038/ismej.2013.225

    Article  CAS  PubMed  Google Scholar 

  80. Meyer B, Kuever J (2007) 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. https://doi.org/10.1128/AEM.01272-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Haruta S, Yoshida T, Aoi Y, Kaneko K, Futamata H (2013) Challenges for complex microbial ecosystems: combination of experimental approaches with mathematical modeling. Microbes Environ 28:285–294. https://doi.org/10.1264/jsme2.ME13034

    Article  PubMed  PubMed Central  Google Scholar 

  82. Middelburg JJ, Levin LA (2009) Coastal hypoxia and sediment biogeochemistry. Biogeosciences 6:1273–1293. https://doi.org/10.5194/bg-6-1273-2009

    Article  CAS  Google Scholar 

  83. Ramsing NB, Kühl M, Jørgensen BB (1993) Distribution of sulfate-reducing bacteria, O2, and H2S in photosynthetic biofilms determined by oligonucleotide probes and microelectrodes. Appl Environ Microbiol 59:3840–3849. https://doi.org/10.1128/AEM.59.11.3840-3849.1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Colin Y, Goñi-Urriza M, Gassie C, Carlier E, Monperrus M, Guyoneaud R (2016) Distribution of sulfate-reducing communities from estuarine to marine bay waters. Microb Ecol 73:39–49. https://doi.org/10.1007/s00248-016-0842-5

    Article  PubMed  Google Scholar 

  85. Kim IN, Min DH (2013) Temporal variation of summertime denitrification rates in the Texas-Louisiana inner shelf region in the Gulf of Mexico: a modeling approach using the extended OMP analysis. Cont Shelf Res 66:49–57. https://doi.org/10.1016/j.csr.2013.07.005

    Article  Google Scholar 

  86. Soto LA, Vázquez-botello A (2013) Legal issues and scientific constraints in the environmental assessment of the Deepwater Horizon oil spill in Mexico Exclusive Economic Zone ( EEZ ) in the Gulf of Mexico. Int J Geosci 4:39–45. https://doi.org/10.4236/ijg.2013.45B007

    Article  Google Scholar 

  87. Krekeler D, Teske A, Cypionka H (1998) Strategies of sulfate-reducing bacteria to escape oxygen stress in a cyanobacterial mat. FEMS Microbiol Ecol 25:89–96. https://doi.org/10.1016/S0168-6496(97)00085-8

    Article  CAS  Google Scholar 

  88. Bade K, Manz W, Szewzyk U (2000) Behavior of sulfate reducing bacteria under oligotrophic conditions and oxygen stress in particle-free systems related to drinking water. FEMS Microbiol Ecol 32:215–223. https://doi.org/10.1111/j.1574-6941.2000.tb00714.x

    Article  CAS  PubMed  Google Scholar 

  89. Cypionka H (2000) Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54:827–848. https://doi.org/10.1146/annurev.micro.54.1.827

    Article  CAS  PubMed  Google Scholar 

  90. Sass AM, Eschemann A, Ku M et al (2002) Growth and chemosensory behavior of sulfate-reducing bacteria in oxygen-sulfide gradients. FEMS Microbiol Ecol 40:47–54. https://doi.org/10.1111/j.1574-6941.2002.tb00935.x

    Article  CAS  PubMed  Google Scholar 

  91. Ramel F, Amrani A, Pieulle L, Lamrabet O, Voordouw G, Seddiki N, Brèthes D, Company M, Dolla A, Brasseur G (2013) Membrane-bound oxygen reductases of the anaerobic sulfate-reducing Desulfovibrio vulgaris Hildenborough: roles in oxygen defence and electron link with periplasmic hydrogen oxidation. Microbiol (United Kingdom) 159:2663–2673. https://doi.org/10.1099/mic.0.071282-0

    Article  CAS  Google Scholar 

  92. Jørgensen BB, Revsbech NP (1989) Oxygen uptake, bacterial distribution, and carbon-nitrogen-sulfur cycling in sediments from the Baltic sea - North Sea transition. Ophelia 31:29–49. https://doi.org/10.1080/00785326.1989.10430849

    Article  Google Scholar 

  93. Wieringa EB, Overman J, Cypionka H (2000) Detection of abundant sulphate-reducing bacteria in marine oxic sediment layers by a combined cultivation and molecular approach. Environ Microbiol 2:417–427. https://doi.org/10.1046/j.1462-2920.2000.00123.x

    Article  CAS  PubMed  Google Scholar 

  94. Lukawska-matuszewska K, Kielczewska J (2016) Effects of near-bottom water oxygen concentration on biogeochemical cycling of C, N and S in sediments of the Gulf of Gdansk (southern Baltic). Cont Shelf Res 117:30–42. https://doi.org/10.1016/j.csr.2016.02.001

    Article  Google Scholar 

  95. Eggleton J, Thomas KV (2004) A review of factors affecting the release and bioavailability of contaminants during sediment disturbance events. Environ Int 30:973–980. https://doi.org/10.1016/j.envint.2004.03.001

    Article  CAS  PubMed  Google Scholar 

  96. Cravo-Laureau C, Duran R (2014) Marine coastal sediments microbial hydrocarbon degradation processes: Contribution of experimental ecology in the omics’era. Front Microbiol 5:1–8. https://doi.org/10.3389/fmicb.2014.00039

    Article  Google Scholar 

  97. Aller RC (1994) Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation. Chem Geol 114:331–345. https://doi.org/10.1016/0009-2541(94)90062-0

    Article  CAS  Google Scholar 

  98. Fischer JP, Ferdelman TG, D’Hondt S et al (2009) Oxygen penetration deep into the sediment of the south pacific gyre. Biogeosciences 6:1467–1478. https://doi.org/10.5194/bg-6-1467-2009

    Article  CAS  Google Scholar 

  99. Jochum LM, Chen X, Lever MA et al (2017) Depth distribution and assembly of sulfate-reducing microbail communities communities in marine sediments of Aarhus Bay. Appl Environ Microbiol 83:1–15. https://doi.org/10.1128/AEM.01547-17

    Article  CAS  Google Scholar 

  100. Vuillemin A, Horn F, Friese A, Winkel M, Alawi M, Wagner D, Henny C, Orsi WD, Crowe SA, Kallmeyer J (2018) Metabolic potential of microbial communities from ferruginous sediments. Environ Microbiol 20:4297–4313. https://doi.org/10.1111/1462-2920.14343

    Article  CAS  PubMed  Google Scholar 

  101. Fichtel J, Koster J, Rullkotter J, Sass H (2008) High variations in endospore numbers within tidal flat sediments revealed by quantification of dipicolinic acid. Geomicrobiol J 25:371–380. https://doi.org/10.1080/01490450802402877

    Article  CAS  Google Scholar 

  102. Gittel A, Mußmann M, Sass H, Cypionka H, Könneke 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. https://doi.org/10.1111/j.1462-2920.2008.01686.x

    Article  CAS  PubMed  Google Scholar 

  103. Lennon JT, Jones SE (2011) Microbial seed banks: The ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130. https://doi.org/10.1038/nrmicro2504

    Article  CAS  PubMed  Google Scholar 

  104. Liu X, Bagwell CE, Wu L, Devol AH, Zhou J (2003) Molecular diversity of sulfate-reducing bacteria from two different continental margin habitats. Appl Environ Microbiol 69:6073–6081. https://doi.org/10.1128/AEM.69.10.6073-6081.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Sawicka JE, Jørgensen BB, Brüchert V (2012) Temperature characteristics of bacterial sulfate reduction in continental shelf and slope sediments. Biogeosciences 9:3425–3435. https://doi.org/10.5194/bg-9-3425-2012

    Article  CAS  Google Scholar 

  106. Celis-Hernandez O, Rosales-Hoz L, Cundy AB, Carranza-Edwards A, Croudace IW, Hernandez-Hernandez H (2018) Historical trace element accumulation in marine sediments from the Tamaulipas shelf, Gulf of Mexico: an assessment of natural vs anthropogenic inputs. Sci Total Environ 622–623:325–336. https://doi.org/10.1016/j.scitotenv.2017.11.228

    Article  CAS  PubMed  Google Scholar 

  107. Cabrera G, Pérez R, Gómez JM et al (2006) Toxic effects of dissolved heavy metals on Desulfovibrio vulgaris and Desulfovibrio sp. strains. J Hazard Mater 135:40–46. https://doi.org/10.1016/j.jhazmat.2005.11.058

    Article  CAS  PubMed  Google Scholar 

  108. Islamud-Din HAE-L, Ahmad A et al (2014) PCR-DGGE and real-time PCR dsrB-based study of the impact of heavy metals on the diversity and abundance of sulfate-reducing bacteria. Biotechnol Bioprocess Eng 19:703–710. https://doi.org/10.1007/s12257-014-0324-x

    Article  CAS  Google Scholar 

  109. Khan S, Hesham AE, Qiao M et al (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res 17:288–296. https://doi.org/10.1007/s11356-009-0134-4

    Article  CAS  Google Scholar 

  110. 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. https://doi.org/10.1016/S0378-1097(98)00122-0

    Article  CAS  Google Scholar 

  111. Gramp JP, Bigham JM, Sasaki K, Tuovinen OH (2007) Formation of Ni- and Zn-sulfides in cultures of sulfate-reducing bacteria. Geomicrobiol J 24:609–614. https://doi.org/10.1080/01490450701758239

    Article  CAS  Google Scholar 

  112. Ni C, Rui J, Huang X et al (2015) High concentrations of bioavailable heavy metals impact freshwater sediment microbial communities. Ann Microbiol 66:1003–1012. https://doi.org/10.1007/s13213-015-1189-8

    Article  CAS  Google Scholar 

  113. Quillet L, Besaury L, Popova M, Paissé S, Deloffre J, Ouddane B (2012) 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. https://doi.org/10.1007/s10126-011-9420-5

    Article  CAS  Google Scholar 

  114. Fortin D, Southam G, Beveridge TJ (1994) Nickel sulfide, iron-nickel sulfide and iron sulfide precipitation by a newly isolated Desulfotomaculum species and its relation to nickel resistance. FEMS Microbiol Ecol 14:121–132. https://doi.org/10.1111/j.1574-6941.1994.tb00099.x

    Article  CAS  Google Scholar 

  115. Caffrey SM, Park HS, Voordouw JK, He Z, Zhou J, Voordouw G (2007) Function of periplasmic hydrogenases in the sulfate-reducing bacterium Desulfovibrio vulgaris hildenborough. J Bacteriol 189:6159–6167. https://doi.org/10.1128/JB.00747-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We are thankful to Gregory Arjona and Francisco Puc for sample collection, and to Abril Gamboa-Muñoz and Victor Ceja for lab assistance. Computational resources used for all bioinformatics analyses were provided by Emanuel Hernández-Núñez. We also are thankful to the anonymous reviewers that help to improve the present manuscript.

Funding

This research has been funded by the Mexican National Council for Science and Technology-Mexican Ministry of Energy Hydrocarbon Fund, project 201441 and CONACYT 251622-2015 received by JQGM. This research was also supported by grants of the “Biotechnology of marine organisms” awarded by the National Council of Science and Technology of Mexico (CONACYT) project 15689-2014. CONACYT awarded MFSSJ with a Ph.D. scholarship. This is a contribution of the Gulf of Mexico Research Consortium (CIGoM).

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Ma. Fernanda Sánchez-Soto generated and designed the experiments, performed the experiments, analyzed the data, prepared the figures and/or tables, authored/reviewed drafts of the paper, and approved the final draft. Daniel Cerqueda-García analyzed the data, prepared the figures and/or tables, authored/reviewed drafts of the paper, and approved the final draft. Rocío J. Alcántara-Hernández and Luisa I. Falcón analyzed the data, contributed to the discussion of the obtained results, authored/reviewed drafts of the paper, and approved the final draft. Daniel Pech and Flor Árcega-Cabrera led the physicochemical analyses, authored/reviewed drafts of the paper, and approved the final draft. Ma. Leopoldina Aguirre-Macedo and José Q. García-Maldonado conceived the research, secured funding, contributed to the discussion of the results, authored contribute to the discussion of the results, reviewed drafts of the paper, and approved the final draft.

Corresponding authors

Correspondence to Ma. Leopoldina Aguirre-Macedo or José Q. García-Maldonado.

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Sánchez-Soto, M.F., Cerqueda-García, D., Alcántara-Hernández, R.J. et al. Assessing the Diversity of Benthic Sulfate-Reducing Microorganisms in Northwestern Gulf of Mexico by Illumina Sequencing of dsrB Gene. Microb Ecol 81, 908–921 (2021). https://doi.org/10.1007/s00248-020-01631-5

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