Cite this paper:
Xiaoyue SONG, Jiangning ZENG, Yi ZHOU, Quanzhen CHEN, Hongsheng YANG, Lu SHOU, Yibo LIAO, Wei HUANG, Ping DU, Qiang LIU. Partial function prediction of sulfate-reducing bacterial community from the rhizospheres of two typical coastal wetland plants in China[J]. Journal of Oceanology and Limnology, 2021, 39(1): 185-197

Partial function prediction of sulfate-reducing bacterial community from the rhizospheres of two typical coastal wetland plants in China

Xiaoyue SONG1, Jiangning ZENG1, Yi ZHOU2,3, Quanzhen CHEN1, Hongsheng YANG2,3, Lu SHOU1, Yibo LIAO1, Wei HUANG1, Ping DU1, Qiang LIU1
1 Key Laboratory of Marine Ecosystem Dynamics, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou 310012, China;
2 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
3 Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
Sulfate-reducing bacteria (SRB) are ubiquitous anaerobic microorganisms that play significant roles in the global biogeochemical cycle. Coastal wetlands, one of the major habitats of SRB, exhibit high sulfate-reducing activity and thus play significant roles in organic carbon remineralization, benthic geochemical action, and plant-microbe interactions. Recent studies have provided credible evidence that the functional rather than the taxonomic composition of microbes responds more closely to environmental factors. Therefore, in this study, functional gene prediction based on PacBio single molecular real-time sequencing of 16S rDNA was applied to determine the sulfate-reducing and organic substrate-decomposing activities of SRB in the rhizospheres of two typical coastal wetland plants in North and South China:Zostera japonica and Scirpus mariqueter. To this end, some physicochemical characteristics of the sediments as well as the phylogenetic structure, community composition, diversity, and proportions of several functional genes of the SRB in the two plant rhizospheres were analyzed. The Z. japonica meadow had a higher dissimilatory sulfate reduction capability than the S. mariqueter-comprising saltmarsh, owing to its larger proportion of SRB in the microbial community, larger proportions of functional genes involved in dissimilatory sulfate reduction, and the stronger ability of the SRB to degrade organic substrates completely. This study confirmed the feasibility of applying microbial community function prediction in research on the metabolic features of SRB, which will be helpful for gaining new knowledge of the biogeochemical and ecological roles of these bacteria in coastal wetlands.
Key words:    sulfate-reducing bacteria (SRB)|microbial community function prediction|16S rDNA PacBio SMRT sequencing|Zostera japonica|Scirpus mariqueter|rhizosphere   
Received: 2019-07-12   Revised: 2019-09-16
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Bahr M, Crump B C, Klepac-Ceraj V, Teske A, Sogin M L, Hobbie J E. 2005. Molecular characterization of sulfatereducing bacteria in a New England salt marsh.Environmental Microbiology, 7(8):l 175-l 185,
Bais H P, Weir T L, Perry L G, Gilroy S, Vivanco J M. 2006.The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57:233-266,
Baldwin D S, Rees G N, Mitchell A M, Watson G, Williams J. 2006. The short-term effects of salinization on anaerobic nutrient cycling and microbial community structure in sediment from a freshwater wetland. Wetlands, 26(2):455-464,[455:tseo so];2.
Barton L L, Fauque G D. 2009. Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Advances in Applied Microbiology, 68:41-98,
Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology, 68(1):1-13,
Blaabjerg V, Mouritsen K N, Finster K. 1998. Diel cycles of sulphate reduction rates in sediments of a Zostera marina bed (Denmark). Aquatic Microbial Ecology, 15(1):97-102,
Bridgham S D, Cadillo-Quiroz H, Keller J K, Zhuang Q L. 2013. Methane emissions from wetlands:biogeochemical, microbial, and modeling perspectives from local to global scales. Global Change Biology, 19(5):1 325-1 346,
Cadillo-Quiroz H, Brauer S, Yashiro E, Sun C, Yavitt J, Zinder S. 2006. Vertical profiles of methanogenesis and methanogens in two contrasting acidic peatlands in central New York State, USA. Environmental Microbiology, 8(8):1 428-1 440,
Cao J L, Yang J X, Hou Q C, Xu H Y, Zheng Y, Zhang H P, Zhang L B. 2017. Assessment of bacterial profiles in aged, home-made Sichuan Paocai brine with varying titratable acidity by PacBio SMRT sequencing technology. Food Control, 78:14-23,
Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QⅡME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5):335-336, 303.
Castro H F, Williams N H, Ogram A. 2000. Phylogeny of sulfate-reducing bacteria. FEMS Microbiology Ecology, 31(1):1-9,
Cifuentes A, Antón J, de Wit R, Rodriguez-Valera F. 2003.Diversity of bacteria and Archaea in sulphate-reducing enrichment cultures inoculated from serial dilution of Zostera noltii rhizosphere samples. Environmental Microbiology, 5(9):754-764,
Cui J, Chen X P, Nie M, Fang S B, Tang B P, Quan Z X, Li B, Fang C M. 2017. Effects of Spartina alterniflora invasion on the abundance, diversity, and community structure of sulfate reducing bacteria along a successional gradient of coastal salt marshes in China. Wetlands, 37(2):221-232,
Devereux R, Mundfrom G W. 1994. A phylogenetic tree of 16S rRNA sequences from sulfate-reducing bacteria in a sandy marine sediment. Applied and Environmental Microbiology, 60(9):3 437-3 439.
Edgar R C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19):2 460-2 461,
Fauque G D. 1995. Ecology of sulfate-reducing bacteria. In:Sulfate-Reducing Bacteria. Springer, Boston, MA. p.217-241.
Friedrich M W. 2002. Phylogenetic analysis reveals multiple lateral transfers of adenosine-5'-phosphosulfate reductase genes among sulfate-reducing microorganisms. Journal of Bacteriology, 184(1):278-289,
Galand P E, Saarnio S, Fritze H, Yrjälä K. 2002. Depth related diversity of methanogen Archaea in Finnish oligotrophic fen. FEMS Microbiology Ecology, 42(3):441-449,
Gibbons S M, Lekberg Y, Mummey D L, Sangwan N, Ramsey P W, Gilbert J A. 2017. Invasive plants rapidly reshape soil properties in a grassland ecosystem. mSystems, 2(7):e00178-16,
Guan J, Xia L P, Wang L Y, Liu J F, Gu J D, Mu B Z. 2013.Diversity and distribution of sulfate-reducing bacteria in four petroleum reservoirs detected by using 16S rRNA and dsrAB genes. International Biodeterioration & Biodegradation, 76:58-66,
Haas B J, Gevers D, Earl A M, Feldgarden M, Ward D V, Giannoukos G, Ciulla D, Tabbaa D, Highlander S K, Sodergren E, Methe B, DeSantis T Z, Petrosino J F, Knight R, Birren B W. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21(3):494-504,
Habicht K S, Salling L, Thamdrup B, Canfield D E. 2005.Effect of low sulfate concentrations on lactate oxidation and isotope fractionation during sulfate reduction by Archaeoglobus fulgidus Strain Z. Applied and Environmental Microbiology, 71(7):3 770-3 777,
Hines M E, Evans R S, Sharak Genthner B R, Willis S G, Friedman S, Rooney-Varga J N, Devereux R. 1999.Molecular phylogenetic and biogeochemical studies of sulfate-reducing bacteria in the rhizosphere of Spartina alterniflora. Applied and Environmental Microbiology, 65(5):2 209-2 216.
Hines M E, Knollmeyer S L, Tugel J B. 1989. Sulfate reduction and other sedimentary biogeochemistry in a northern New England salt marsh. Limnology and Oceanography, 34(3):578-590,
Hou Q C, Xu H Y, Zheng Y, Xi X X, Kwok L Y, Sun Z H, Zhang H P, Zhang W Y. 2015. Evaluation of bacterial contamination in raw milk, ultra-high temperature milk and infant formula using single molecule, real-time sequencing technology. Journal of Dairy Science, 98(12):8 464-8 472,
Howarth R W. 1993. Microbial processes in salt-marsh sediments. In:Ford T E ed. Aquatic Microbiology:an Ecological Approach. Blackwell Scientific Publications, Boston. p.239-260.
Itoh T, Suzuki K I, Nakase T. 1998. Thermocladium modestius gen. nov., sp. nov., a new genus of rod-shaped, extremely thermophilic crenarchaeote. International Journal of Systematic Bacteriology, 48(3):879-887,
Itoh T, Suzuki K I, Sanchez P C, Nakase T. 1999. Caldivirga maquilingensis gen. nov., sp. nov., a new genus of rodshaped crenarchaeote isolated from a hot spring in the Philippines. International Journal of Systematic Bacteriology, 49(3):1 157-1 163,
Jørgensen B B. 1982. Mineralization of organic matter in the sea bed-the role of sulphate reduction. Nature, 296(5858):643-645,
Kim M, Oh H S, Park S C, Chun J. 2014. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 64:346-351,
Klepac-Ceraj V, Bahr M, Crump B C, Teske A P, Hobbie J E, Polz M F. 2004. High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria. Environmental Microbiology, 6(7):686-698,
Kotiaho M, Fritze H, Merilä P, Juottonen H, Leppälä M, Laine J, Laiho R, Yrjälä K, Tuittila E S. 2010. Methanogen activity in relation to water table level in two boreal fens.Biology and Fertility of Soils, 46(6):567-575,
Langille M I G, Zaneveld J, Caporaso J G, McDonald D, Knights D, Reyes J A, Clemente J C, Burkepile D E, Vega T R L, Knight R, Beiko R G, Huttenhower C. 2013.Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology, 31(9):814-824,
Larsen S, Nielsen L P, Schramm A. 2015. Cable bacteria associated with long-distance electron transport in New England salt marsh sediment. Environmental Microbiology, 7(2):175-179,
Liu W J, Zheng Y, Kwok L Y, Sun Z H, Zhang J C, Guo Z, Hou Q C, Menhe B, Zhang H P. 2015. High-throughput sequencing for the detection of the bacterial and fungal diversity in Mongolian naturally fermented cow's milk in Russia. BMC Microbiology, 15:45,
Louca S, Parfrey L W, Doebeli M. 2016. Decoupling function and taxonomy in the global ocean microbiome. Science, 353(6305):1 272-1 277,
Lücker S, Steger D, Kjeldsen K U, MacGregor B J, Wagner M, Loy A. 2007. Improved 16S rRNA-targeted probe set for analysis of sulfate-reducing bacteria by fluorescence in situ hybridization. Journal of Microbiological Methods, 69(3):523-528,
Moreau J W, Zierenberg R A, Banfield J F. 2010. Diversity of dissimilatory sulfite reductase genes (dsrAB) in a salt marsh impacted by long-term acid mine drainage. Applied and Environmental Microbiology, 76(14):4 819-4 828,
Mori K, Kim H, Kakegawa T, Hanada S. 2003. A novel lineage of sulfate-reducing microorganisms:Thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp. nov., a new thermophilic isolate from a hot spring. Extremophiles, 7(4):283-290,
Mosher J J, Bernberg E L, Shevchenko O, Kan J, Kaplan L A. 2013. Efficacy of a 3rd generation high-throughput sequencing platform for analyses of 16S rRNA genes from environmental samples. Journal of Microbiological Methods, 95(2):175-181,
Muyzer G, Stams A J M. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nature Reviews Microbiology, 6(6):441-454,
Nielsen L B, Finster K, Welsh D T, Donelly A, Herbert R A, De Wit R, Lomstein B A A. 2001. Sulphate reduction and nitrogen fixation rates associated with roots, rhizomes and sediments from Zostera noltii and Spartina maritima meadows. Environmental Microbiology, 3(1):63-71,
Nielsen L P, Risgaard-Petersen N, Fossing H, Christensen P B, Sayama M. 2010. Electric currents couple spatially separated biogeochemical processes in marine sediment.Nature, 463(7284):1 071-1 074,
Ollivier B, Cayol J L, Fauque G. 2007. Sulphate-reducing bacteria from oil field environments and deep-sea hydrothermal vents. In:Barton L L, Hamilton W A eds.Sulphate-Reducing Bacteria:Environmental and Engineered Systems. Cambridge University Press, Cambridge. p.305-328.
Pester M, Knorr K H, Friedrich M W, Wagner M, Loy A. 2012.Sulfate-reducing microorganisms in wetlands-fameless actors in carbon cycling and climate change. Frontiers in Microbiology, 3:72,
Poffenbarger H J, Needelman B A, Megonigal J P. 2011.Salinity influence on methane emissions from tidal marshes. Wetlands, 31(5):831-842,
Rabus R, Hansen T A, Widdel F. 2006. Dissimilatory sulfateand sulfur-reducing prokaryotes. In:Dworkin M, Falkow S, Rosenberg E, Schleifer K H, Stackebrandt E eds. The Prokaryotes, Vol. 2:Ecophysiology and Biochemistry.Springer, Berlin. p.659-768.
Rambaut A. 2016. FigTree v1.4.3 software. Institute of Evolutionary Biology, University of Edinburgh.Rooney-Varga J N, Devereux R, Evans R S, Hines M E. 1997.Seasonal changes in the relative abundance of uncultivated sulfate-reducing bacteria in a salt marsh sediment and in the rhizosphere of Spartina alterniflora. Applied and Environmental Microbiology, 63(10):3 895-3 901.
Schauer R, Risgaard-Petersen N, Kjeldsen K U, Tataru Bjerg J J, Jørgensen B B, Schramm A, Nielsen L P. 2014.Succession of cable bacteria and electric currents in marine sediment. ISME Journal, 8(6):1 314-1 322,
She C X, Zhang Z C, Cadillo-Quiroz H, Tong C. 2016. Factors regulating community composition of methanogens and sulfate-reducing bacteria in brackish marsh sediments in the Min River estuary, southeastern China. Estuarine, Coastal and Shelf Science, 181:27-38,
Shen Y, Buick R. 2004. The antiquity of microbial sulfate reduction. Earth-Science Reviews, 64(3-4):243-272,
Silvestro D, Michalak I. 2012. RaxmlGUI:a graphical frontend for RAxML. Organisms Diversity & Evolution, 12(4):335-337,
Smith J M, Green S J, Kelley C A, Prufert-Bebout L, Bebout B M. 2008. Shifts in methanogen community structure and function associated with long-term manipulation of sulfate and salinity in a hypersaline microbial mat.Environmental Microbiology, 10(2):386-394,
Steudler P A, Peterson B J. 1984. Contribution of gaseous Sulphur from salt marshes to the global Sulphur cycle.Nature, 311(5985):455-457,
Sulu-Gambari F, Seitaj D, Meysman F J R, Schauer R, Polerecky L, Slomp C P. 2016. Cable bacteria control ironphosphorus dynamics in sediments of a coastal hypoxic basin. Environmental Science & Technology, 50(3):1 227-1 233,
Wagner M, Amann R, Lemmer H, Schleifer K H. 1993.Probing activated sludge with oligonucleotides specific for proteobacteria:inadequacy of culture-dependent methods for describing microbial community structure.Applied and Environmental Microbiology, 59(5):1 520-1 525.
Welsh D T, Bourguès S, De Wit R, Auby I. 1997. Effect of plant photosynthesis, carbon sources and ammonium availability on nitrogen fixation rates in the rhizosphere of Zostera noltii. Aquatic Microbial Ecology, 12(3):285-290,
Yuan H W, Chen J F, Ye Y, Lou Z H, Jin A M, Chen X G, Jiang Z P, Lin Y S, Chen C T A, Loh P S. 2017. Sources and distribution of sedimentary organic matter along the Andong salt marsh, Hangzhou Bay. Journal Marine Systems, 174:78-88, 2017.06.001.
Zeleke J, Sheng Q, Wang J G, Huang M Y, Xia F, Wu J H, Quan Z X. 2013. Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments. Frontiers in Microbiology, 4:243,
Zhang X M, Zhou Y, Liu P, Wang F, Liu B J, Liu X J, Yang H S. 2015. Temporal pattern in biometrics and nutrient stoichiometry of the intertidal seagrass Zostera japonica and its adaptation to air exposure in a temperate marine lagoon (China):implications for restoration and management. Marine Pollution Bulletin, 94(1-2):103-113,
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