Characterization of microbial communities in sediments of the South Yellow Sea

Abstract

Illumina sequencing and quantitative PCR (qPCR) based on the 16S ribosomal RNA (rRNA) gene were conducted to characterize the vertical distribution of bacterial and archaeal communities in the sediments of two sites from the South Yellow Sea. Both bacterial and archaeal communities showed a clear stratified distribution with sediment depth. The microbial communities in the upper layers were distinct from those in the deeper layers; the relative abundances of sequences of Thaumarchaeota, Gammaproteobacteria, and Actinobacteria were higher in the upper than in the deeper sediments, whereas the sequences of Bathyarchaeia, Lokiarchaeota, Euryarchaeota, Chloroflexi, and Deltaproteobacteria were relatively more abundant in the deeper sediments. Sediment depth and total organic carbon (TOC) can significantly influence both the bacterial and archaeal communities. Furthermore, bacterial and archaeal groups potentially involved in nitrogen, sulfur, and methane metabolism were detected in both sites. In our study, both ammonia-oxidizing bacteria (Nitrospira) and ammonia-oxidizing archaea (Candidatus Nitrosopumilus) were responsible for ammonia oxidization. Additionally, sulfur-reducing bacteria SEEP-SRB1 forming consortia with anaerobic methane-oxidizing archaea ANME-2a-2b were capable of anaerobic methane oxidation (AOM) in the 3400-02 sediment samples.

This is a preview of subscription content, access via your institution.

References

  1. Bagchi A, Roy D, Roy P. 2005. Homology modeling of a transcriptional regulator SoxR of the Lithotrophic sulfur oxidation (Sox) operon in α-Proteobacteria. Journal of Biomolecular Structure and Dynamics, 22(5): 571–577. https://doi.org/10.1080/07391102.2005.10507027.

    Article  Google Scholar 

  2. Berg C, Listmann L, Vandieken V, Vogts A, Jürgens K. 2014. Chemoautotrophic growth of ammonia-oxidizing Thaumarchaeota enriched from a pelagic redox gradient in the Baltic Sea. Frontiers in Microbiology, 5: 786, https://doi.org/10.3389/fmicb.2014.00786.

    Google Scholar 

  3. Berlanga M, Aas J A, Paster B J, Boumenna T, Dewhirst F E, Guerrero R. 2008. Phylogenetic diversity and temporal variation in the Spirochaeta populations from two Mediterranean microbial mats. International Microbiology, 11(4): 267–274, https://doi.org/10.2436/20.1501.01.71.

    Google Scholar 

  4. Biddle J F, Lipp J S, Lever M A, Lloyd K G, Sorensen K B, Anderson R, Fredricks H F, Elvert M, Kelly T J, Schrag D P, Sogin M L, Brenchley J E, Teske A, House C H, Hinrichs K U. 2006. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proceedings of the National Academy of Sciences of the United States of America, 103(10): 3 846–3 851, https://doi.org/10.1073/pnas.0600035103.

    Article  Google Scholar 

  5. Boetius A, Ravenschlag K, Schubert C J, Rickert D, Widdel F, Gieseke A, Amann R, Jørgensen B B, Witte U, Pfannkuche O. 2000. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature, 407(6804): 623–626, https://doi.org/10.1038/35036572.

    Article  Google Scholar 

  6. Bokulich N A, Subramanian S, Faith J J, Gevers D, Gordon J I, Knight R, Mills D A, Caporaso J G. 2013. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10(1): 57–59, https://doi.org/10.1038/nmeth.2276.

    Article  Google Scholar 

  7. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. 2008. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Reviews Microbiology, 6(3): 245–252, https://doi.org/10.1038/nrmicro1852.

    Article  Google Scholar 

  8. Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J A, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6(8): 1 621–1 624, https://doi.org/10.1038/ismej.2012.8.

    Article  Google Scholar 

  9. Coolen M J L, Hopmans EC, Rijpstra WIC, Muyzer G, Schouten S, Volkman J K, Damsté JSS. 2004. Evolution of the methane cycle in Ace Lake (Antarctica) during the Holocene: response of methanogens and methanotrophs to environmental change. Organic Geochemistry, 35(10): 1 151–1 167, https://doi.org/10.1016/j.orggeochem.2004.06.009.

    Article  Google Scholar 

  10. Covault J A, Fildani A. 2014. Continental shelves as sediment capacitors or conveyors: source-to-sink insights from the tectonically active Oceanside shelf, southern California, USA. Geological Society, London, Memoirs, 41(1): 315–326, https://doi.org/10.1144/M41.23.

    Article  Google Scholar 

  11. Cowie G L, Hedges J I. 1994. Biochemical indicators of diagenetic alteration in natural organic matter mixtures. Nature, 369(6478): 304–307, https://doi.org/10.1038/369304a0.

    Article  Google Scholar 

  12. DeLong E F. 1992. Archaea in coastal marine environments. Proceedings of the National Academy of Sciences of the United States of America, 89(12): 5 685–5 689, https://doi.org/10.1073/pnas.89.12.5685.

    Article  Google Scholar 

  13. Devereux R, Mosher J J, Vishnivetskaya T A, Brown S D, Beddick D L Jr, Yates D F, Palumbo A V. 2015. Changes in northern Gulf of Mexico sediment bacterial and archaeal communities exposed to hypoxia. Geobiology, 13(5): 478–493, https://doi.org/10.1111/gbi.12142.

    Article  Google Scholar 

  14. Dharamshi J E, Tamarit D, Eme L, Stairs C W, Martijn J, Homa F, Jørgensen S L, Spang A, Ettema T J G. 2020. Marine sediments illuminate Chlamydiae diversity and evolution. Current Biology, 30(6): 1 032–1 048.e7, https://doi.org/10.1016/j.cub.2020.02.016.

    Article  Google Scholar 

  15. Dong Y, Zhao Y, Zhang W Y, Li Y, Zhou F, Liu C G, Wu Y, Liu S M, Zhang W C, Xiao T. 2014. Bacterial diversity and community structure in the East China Sea by 454 sequencing of the 16S rRNA gene. Chinese Journal of Oceanology and Limnology, 32(3): 527–541, https://doi.org/10.1007/s00343-014-3215-2.

    Article  Google Scholar 

  16. Durbin A M, Teske A. 2012. Archaea in organic-lean and organic-rich marine subsurface sediments: an environmental gradient reflected in distinct phylogenetic lineages. Frontiers in Microbiology, 3: 168, https://doi.org/10.3389/fmicb.2012.00168.

    Article  Google Scholar 

  17. Evans P N, Parks D H, Chadwick G L, Robbins S J, Orphan V J, Golding S D, Tyson G W. 2015. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science, 350(6259): 434–438, https://doi.org/10.1126/science.aac7745.

    Article  Google Scholar 

  18. Fernández-Gómez B, Richter M, Schüler M, Pinhassi J, Acinas S G, González J M, Pedrós-Alió C. 2013. Ecology of marine Bacteroidetes: a comparative genomics approach. The ISME Journal, 7(5): 1 026–1 037, https://doi.org/10.1038/ismej.2012.169.

    Article  Google Scholar 

  19. Fuhrman J A, Davis A A. 1997. Widespread archaea and novel bacteria from the deep sea as shown by 16S rRNA gene sequences. Marine Ecology Progress Series, 150(1): 275–285, https://doi.org/10.3354/meps150275.

    Article  Google Scholar 

  20. Fuhrman J A. 2009. Microbial community structure and its functional implications. Nature, 459(7244): 193–199, https://doi.org/10.1038/nature08058.

    Article  Google Scholar 

  21. Gauthier M E A, Watson J R, Degnan S M. 2016. Draft genomes shed light on the dual bacterial symbiosis that dominates the microbiome of the coral reef sponge Amphimedon queenslandica. Frontiers in Marine Science, 3: 196, https://doi.org/10.3389/fmars.2016.00196.

    Article  Google Scholar 

  22. Gold T. 1992. The deep, hot biosphere. Proceedings of the National Academy of Sciences of the United States of America, 89(13): 6 045–6 049, https://doi.org/10.1073/pnas.89.13.6045.

    Article  Google Scholar 

  23. Graham D E, Wallenstein M D, Vishnivetskaya T A, Waldrop M P, Phelps T J, Pfiffner S M, Onstott T C, Whyte L G, Rivkina E M, Gilichinsky D A, Elias D A, Mackelprang R, VerBerkmoes N C, Hettich R L, Wagner D, Wullschleger S D, Jansson J K. 2012. Microbes in thawing permafrost: the unknown variable in the climate change equation. The ISME Journal, 6(4): 709–712, https://doi.org/10.1038/ismej.2011.163.

    Article  Google Scholar 

  24. He H, Zhen Y, Mi T Z, Fu L L, Yu Z G. 2018. Ammonia-oxidizing archaea and bacteria differentially contribute to ammonia oxidation in sediments from adjacent waters of Rushan Bay, China. Frontiers in Microbiology, 9: 116, https://doi.org/10.3389/fmicb.2018.00116.

    Article  Google Scholar 

  25. He H, Zhen Y, Mi T Z, Yu Z G. 2016a. Community composition and abundance of ammonia-oxidizing archaea in sediments from the Changjiang Estuary and its adjacent area in the East China Sea. Geomicrobiology Journal, 33(5): 416–425, https://doi.org/10.1080/01490451.2014.986695.

    Article  Google Scholar 

  26. He Y, Li M, Perumal V, Feng X, Fang J, Xie J, Sievert S M, Wang F. 2016b. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nature Microbiology, 1(6): 16 035, https://doi.org/10.1038/nmicrobiol.2016.35.

    Article  Google Scholar 

  27. Ho A, Angel R, Veraart A J, Daebeler A, Jia Z J, Kim S Y, Kerckhof F M, Boon N, Bodelier P L E. 2016. Biotic interactions in microbial communities as modulators of biogeochemical processes: methanotrophy as a model system. Frontiers in Microbiology, 7: 1 285, https://doi.org/10.3389/fmicb.2016.01285.

    Article  Google Scholar 

  28. Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, Suzuki M, Takai K, Delwiche M, Colwell F S, Nealson K H, Horikoshi K, D’Hondt S, Jørgensen B B. 2006. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proceedings of the National Academy of Sciences of the United States of America, 103(8): 2 815–2 820, https://doi.org/10.1073/pnas.0511033103.

    Article  Google Scholar 

  29. Jiang L J, Zheng Y P, Chen J Q, Xiao X, Wang F P. 2011. Stratification of archaeal communities in shallow sediments of the Pearl River Estuary, Southern China. Antonie Van Leeuwenhoek, 99(4): 739–751, https://doi.org/10.1007/s10482-011-9548-3.

    Article  Google Scholar 

  30. Karner M B, DeLong E F, Karl D M. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature, 409(6819): 507–510, https://doi.org/10.1038/35054051.

    Article  Google Scholar 

  31. Lazar C S, Baker B J, Seitz K, Hyde A S, Dick G J, Hinrichs K U, Teske A P. 2016. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environmental Microbiology, 18(4): 1 200–1 211, https://doi.org/10.1111/1462-2920.13142.

    Article  Google Scholar 

  32. Lee C K, Barbier B A, Bottos E M, McDonald I R, Cary S C. 2012. The inter-valley soil comparative survey: the ecology of Dry Valley edaphic microbial communities. The ISME Journal, 6(5): 1 046–1 057, https://doi.org/10.1038/ismej.2011.170.

    Article  Google Scholar 

  33. Lenk S, Arnds J, Zerjatke K, Musat N, Amann R, Mußmann M. 2011. Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment. Environmental Microbiology, 13(3): 758–774, https://doi.org/10.1111/j.1462-2920.2010.02380.x.

    Article  Google Scholar 

  34. Lentini V, Gugliandolo C, Bunk B, Overmann J, Maugeri T L. 2014. Diversity of prokaryotic community at a shallow marine hydrothermal site elucidated by Illumina sequencing technology. Current Microbiology, 69(4): 457–466, https://doi.org/10.1007/s00284-014-0609-5.

    Article  Google Scholar 

  35. Lin X J, Handley K M, Gilbert J A, Kostka J E. 2015. Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat. The ISME Journal, 9(12): 2 740–2 744, https://doi.org/10.1038/ismej.2015.77.

    Article  Google Scholar 

  36. Liu C S, Zhao D F, Yan L H, Wang A J, Gu Y Y, Lee D J. 2015a. Elemental sulfur formation and nitrogen removal from wastewaters by autotrophic denitrifiers and anammox bacteria. Bioresource Technology, 191: 332–336, https://doi.org/10.1016/j.biortech.2015.05.027.

    Article  Google Scholar 

  37. Liu J W, Liu X S, Wang M, Qiao Y L, Zheng Y F, Zhang X H. 2015b. Bacterial and archaeal communities in sediments of the North Chinese Marginal Seas. Microbial Ecology, 70(1): 105–117, https://doi.org/10.1007/s00248-014-0553-8.

    Article  Google Scholar 

  38. Liu Y C, Whitman W B. 2008. Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Annals of the New York Academy of Sciences, 1125(1): 171–189, https://doi.org/10.1196/annals.1419.019.

    Article  Google Scholar 

  39. Lloyd K G, Schreiber L, Petersen D G, Kjeldsen K U, Lever M A, Steen A D, Stepanauskas R, Richter M, Kleindienst S, Lenk S, Schramm A, Jørgensen B B. 2013. Predominant archaea in marine sediments degrade detrital proteins. Nature, 496(7444): 215–218, https://doi.org/10.1038/nature12033.

    Article  Google Scholar 

  40. Lovley D R, Klug M J. 1983. Sulfate reducers can outcompete methanogens at freshwater sulfate concentrations. Applied and Environmental Microbiology, 45(1): 187–192, https://doi.org/10.1128/AEM.45.1.187-192.1983.

    Article  Google Scholar 

  41. Lozada M, Marcos M S, Commendatore M G, Gil M N, Dionisi H M. 2014. The bacterial community structure of hydrocarbon-polluted marine environments as the basis for the definition of an ecological index of hydrocarbon exposure. Microbes and Environments, 29(3): 269–276, https://doi.org/10.1264/jsme2.ME14028.

    Article  Google Scholar 

  42. Magoč T, Salzberg S L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2 957–2 963, https://doi.org/10.1093/bioinformatics/btr507.

    Article  Google Scholar 

  43. Mahmoudi N, Robeson M S, Castro H F, Fortney J L, Techtmann S M, Joyner D C, Paradis C J, Pfiffner S M, Hazen T C. 2015. Microbial community composition and diversity in Caspian Sea sediments. FEMS Microbiology Ecology, 91(1): 1–11, https://doi.org/10.1093/femsec/fiu013.

    Article  Google Scholar 

  44. Niemann H, Lösekann T, De Beer D, Elvert M, Nadalig T, Knittel K, Amann R, Sauter E J, Schlüter M, Klages M, Foucher J P, Boetius A. 2006. Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature, 443(7113): 854–858, https://doi.org/10.1038/nature05227.

    Article  Google Scholar 

  45. Nunoura T, Takaki Y, Kazama H, Hirai M, Ashi J, Imachi H, Takai K. 2012. Microbial diversity in deep-sea methane seep sediments presented by SSU rRNA gene tag sequencing. Microbes and Environments, 27(4): 382–390, https://doi.org/10.1264/jsme2.ME12032.

    Article  Google Scholar 

  46. Offre P, Spang A, Schleper C. 2013. Archaea in biogeochemical cycles. Annual Review of Microbiology, 67(1): 437–457, https://doi.org/10.1146/annurev-micro-092412-155614.

    Article  Google Scholar 

  47. Oni O E, Schmidt F, Miyatake T, Kasten S, Witt M, Hinrichs K U, Friedrich M W. 2015. Microbial communities and organic matter composition in surface and subsurface sediments of the Helgoland mud area, North Sea. Frontiers in Microbiology, 6: 1 290, https://doi.org/10.3389/fmicb.2015.01290.

    Google Scholar 

  48. Orphan V J, House C H, Hinrichs K U, McKeegan K D, DeLong E F. 2002. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proceedings of the National Academy of Sciences of the United States of America, 99(11): 7 663–7 668, https://doi.org/10.1073/pnas.072210299.

    Article  Google Scholar 

  49. Pala C, Molari M, Nizzoli D, Bartoli M, Viaroli P, Manini E. 2018. Environmental drivers controlling bacterial and archaeal abundance in the sediments of a Mediterranean lagoon ecosystem. Current Microbiology, 75(9): 1 147–1 155, https://doi.org/10.1007/s00284-018-1503-3.

    Article  Google Scholar 

  50. Peiffer J A, Spor A, Koren O, Jin Z, Tringe S G, Dangl J L, Buckler E S, Ley R E. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America, 110(16): 6 548–6 553, https://doi.org/10.1073/pnas.1302837110.

    Article  Google Scholar 

  51. Porat I, Vishnivetskaya T A, Mosher J J, Brandt C C, Yang Z K, Brooks S C, Liang L Y, Drake M M, Podar M, Brown S D, Palumbo A V. 2010. Characterization of archaeal community in contaminated and uncontaminated surface stream sediments. Microbial Ecology, 60(4): 784–795, https://doi.org/10.1007/s00248-010-9734-2.

    Article  Google Scholar 

  52. Poulsen M, Schwab C, Jensen B B, Engberg R M, Spang A, Canibe N, Højberg O, Milinovich G, Fragner L, Schleper C, Weckwerth W, Lund P, Schramm A, Urich T. 2013. Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nature Communications, 4: 1 428, https://doi.org/10.1038/ncomms2847.

    Article  Google Scholar 

  53. Qiao Y L, Liu J W, Zhao M X, Zhang X H. 2018. Sediment depth-dependent spatial variations of bacterial communities in mud deposits of the eastern China marginal seas. Frontiers in Microbiology, 9: 1 128, https://doi.org/10.3389/fmicb.2018.01128.

    Article  Google Scholar 

  54. Reed A J, Lutz R A, Vetriani C. 2006. Vertical distribution and diversity of bacteria and archaea in sulfide and methanerich cold seep sediments located at the base of the Florida Escarpment. Extremophiles, 10(3): 199–211, https://doi.org/10.1007/s00792-005-0488-6.

    Article  Google Scholar 

  55. Robador A, Müller A L, Sawicka J E, Berry D, Hubert C R J, Loy A, Jørgensen B B, Brüchert V. 2016. Activity and community structures of sulfate-reducing microorganisms in polar, temperate and tropical marine sediments. The ISME Journal, 10(4): 796–809, https://doi.org/10.1038/ismej.2015.157.

    Article  Google Scholar 

  56. Säwström C, Serrano O, Rozaimi M, Lavery P S. 2016. Utilization of carbon substrates by heterotrophic bacteria through vertical sediment profiles in coastal and estuarine seagrass meadows. Environmental Microbiology Reports, 8(5): 582–589, https://doi.org/10.1111/1758-2229.12406.

    Article  Google Scholar 

  57. Schippers A, Kock D, Höft C, Köweker G, Siegert M. 2012. Quantification of microbial communities in subsurface marine sediments of the Black Sea and off Namibia. Frontiers in Microbiology, 3: 16, https://doi.org/10.3389/fmicb.2012.00016.

    Article  Google Scholar 

  58. Schippers A, Neretin L N. 2006. Quantification of microbial communities in near-surface and deeply buried marine sediments on the Peru continental margin using real-time PCR. Environmental Microbiology, 8(7): 1 251–1 260, https://doi.org/10.1111/j.1462-2920.2006.01019.x.

    Article  Google Scholar 

  59. Schönheit P, Kristjansson J K, Thauer R K. 1982. Kinetic mechanism for the ability of sulfate reducers to outcompete methanogens for acetate. Archives of Microbiology, 132(3): 285–288, https://doi.org/10.1007/BF00407967.

    Article  Google Scholar 

  60. Shehab N, Li D, Amy G L, Logan B E, Saikaly P E. 2013. Characterization of bacterial and archaeal communities in air-cathode microbial fuel cells, open circuit and sealed-off reactors. Applied Microbiology and Biotechnology, 97(22): 9 885–9 895, https://doi.org/10.1007/s00253-013-5025-4.

    Article  Google Scholar 

  61. Shi X F, Shen S X, Yi H I, Chen Z H, Meng Y. 2003. Modern sedimentary environments and dynamic depositional systems in the southern Yellow Sea. Chinese Science Bulletin, 48(S1): 1–7, https://doi.org/10.1007/BF02900933.

    Article  Google Scholar 

  62. Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E, Streit W, Stahl D A, Wagner M, Schleper C. 2010. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends in Microbiology, 18(8): 331–340, https://doi.org/10.1016/j.tim.2010.06.003.

    Article  Google Scholar 

  63. Spring S, Riedel T, Spröer C, Yan S, Harder J, Fuchs B M. 2013. Taxonomy and evolution of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria: description of Luminiphilus syltensis gen. nov., sp. nov., reclassification of Haliea rubra as Pseudohaliea rubra gen. nov., comb. nov., and emendation of Chromatocurvus halotolerans. BMC Microbiology, 13(1): 118, https://doi.org/10.1186/1471-2180-13-118.

    Article  Google Scholar 

  64. Stahl D A, de la Torre J R. 2012. Physiology and diversity of ammonia-oxidizing archaea. Annual Review of Microbiology, 66(1): 83–101, https://doi.org/10.1146/annurev-micro-092611-150128.

    Article  Google Scholar 

  65. Sun W M, Xiao E Z, Pu Z L, Krumins V, Dong Y R, Li B Q, Hu M. 2018. Paddy soil microbial communities driven by environment- and microbe-microbe interactions: a case study of elevation-resolved microbial communities in a rice terrace. Science of the Total Environment, 612: 884–893, https://doi.org/10.1016/j.scitotenv.2017.08.275.

    Article  Google Scholar 

  66. Suzuki D, Li Z L, Cui X X, Zhang C F, Katayama A. 2014. Reclassification of Desulfobacterium anilini as Desulfatiglans anilini comb. nov. within Desulfatiglans gen. nov., and description of a 4-chlorophenol-degrading sulfate-reducing bacterium, Desulfatiglans parachlorophenolica sp. nov. International Journal of Systematic and Evolutionary Microbiology, 64(Pt 9): 3 081–3 086, https://doi.org/10.1099/ijs.0.064360-0.

    Article  Google Scholar 

  67. Timmers P H A, Suarez-Zuluaga D A, van Rossem M, Diender M, Stams A J M, Plugge C M. 2016. Anaerobic oxidation of methane associated with sulfate reduction in a natural freshwater gas source. The ISME Journal, 10(6): 1 400–1 412, https://doi.org/10.1038/ismej.2015.213.

    Article  Google Scholar 

  68. Tringe S G, Hugenholtz P. 2008. A renaissance for the pioneering 16S rRNA gene. Current Opinion in Microbiology, 11(5): 442–446, https://doi.org/10.1016/j.mib.2008.09.011.

    Article  Google Scholar 

  69. Urakawa H, Yoshida T, Nishimura M, Ohwada K. 2000. Characterization of depth-related population variation in microbial communities of a coastal marine sediment using 16S rDNA-based approaches and quinone profiling. Environmental Microbiology, 2(5): 542–554, https://doi.org/10.1046/j.1462-2920.2000.00137.x.

    Article  Google Scholar 

  70. Valentine D L. 2002. Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Antonie van Leeuwenhoek, 81(1–4): 271–282, https://doi.org/10.1023/A:1020587206351.

    Article  Google Scholar 

  71. Varon-Lopez M, Dias A C F, Fasanella C C, Durrer A, Melo I S, Kuramae E E, Andreote F D. 2014. Sulphur-oxidizing and Sulphate-reducing communities in Brazilian mangrove sediments. Environmental Microbiology, 16(3): 845–855, https://doi.org/10.1111/1462-2920.12237.

    Article  Google Scholar 

  72. Wakeham S G, Lee C, Hedges J I, Hernes P J, Peterson M J. 1997. Molecular indicators of diagenetic status in marine organic matter. Geochimica et Cosmochimica Acta, 61(24): 5 363–5 369, https://doi.org/10.1016/S0016-7037(97)00312-8.

    Article  Google Scholar 

  73. Walsh J J. 1991. Importance of continental margins in the marine biogeochemical cycling of carbon and nitrogen. Nature, 350(6313): 53–55, https://doi.org/10.1038/350053a0.

    Article  Google Scholar 

  74. Wang Y, Sheng H F, He Y, Wu J Y, Jiang Y X, Tam N F Y, Zhou H W. 2012. Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina tags. Applied and Environmental Microbiology, 78(23): 8 264–8 271, https://doi.org/10.1128/AEM.01821-12.

    Article  Google Scholar 

  75. Wilms R, Kopke B, Sass H, Chang T S, Cypionka H, Engelen B. 2006. Deep biosphere-related bacteria within the subsurface of tidal flat sediments. Environmental Microbiology, 8(4): 709–719, https://doi.org/10.1111/j.1462-2920.2005.00949.x.

    Article  Google Scholar 

  76. Xiao K Q, Beulig F, Røy H, Jørgensen B B, Risgaard-Petersen N. 2018. Methylotrophic methanogenesis fuels cryptic methane cycling in marine surface sediment. Limnology and Oceanography, 63(4): 1 519–1 527, https://doi.org/10.1002/lno.10788.

    Article  Google Scholar 

  77. Xiong J B, Ye X S, Wang K, Chen H P, Hu C J, Zhu J L, Zhang D M. 2014. Biogeography of the sediment bacterial community responds to a nitrogen pollution gradient in the East China Sea. Applied and Environmental Microbiology, 80(6): 1 919–1 925, https://doi.org/10.1128/AEM.03731-13.

    Article  Google Scholar 

  78. Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, Harada H, Kamagata Y. 2006. Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. International Journal of Systematic and Evolutionary Microbiology, 56(6): 1 331–1 340, https://doi.org/10.1099/ijs.0.64169-0.

    Article  Google Scholar 

  79. Yu S L, Yao P, Liu J W, Zhao B, Zhang G L, Zhao M X, Yu Z G, Zhang X H. 2016. Diversity, abundance, and niche differentiation of ammonia-oxidizing prokaryotes in mud deposits of the eastern China marginal Seas. Frontiers in Microbiology, 7: 137, https://doi.org/10.3389/fmicb.2016.00137.

    Google Scholar 

  80. Zhang Y, Wang X G, Zhen Y, Mi T Z, He H, Yu Z G. 2017. Microbial diversity and community structure of sulfate-reducing and sulfur-oxidizing bacteria in sediment cores from the East China Sea. Frontiers in Microbiology, 8: 2133, https://doi.org/10.3389/fmicb.2017.02133.

    Article  Google Scholar 

  81. Zhou Z C, Meng H, Liu Y, Gu J D, Li M. 2017. Stratified bacterial and archaeal community in mangrove and intertidal wetland mudflats revealed by high throughput 16S rRNA gene sequencing. Frontiers in Microbiology, 8: 2148, https://doi.org/10.3389/fmicb.2017.02148.

    Article  Google Scholar 

  82. Zhu D C, Tanabe S H, Yang C, Zhang W M, Sun J Z. 2013. Bacterial community composition of South China Sea sediments through pyrosequencing-based analysis of 16S rRNA genes. PLoS One, 8(10): e78501, https://doi.org/10.1371/journal.pone.0078501.

    Article  Google Scholar 

  83. Zhuang G C, Heuer V B, Lazar C S, Goldhammer T, Wendt J, Samarkin V A, Elvert M, Teske A P, Joye S B, Hinrichs K U. 2018. Relative importance of methylotrophic methanogenesis in sediments of the western Mediterranean Sea. Geochimica et Cosmochimica Acta, 224: 171–186, https://doi.org/10.1016/j.gca.2017.12.024.

    Article  Google Scholar 

  84. Zinger L, Amaral-Zettler L A, Fuhrman J A, Horner-Devine M C, Huse S M, Welch D B M, Martiny J B H, Sogin M, Boetius A, Ramette A. 2011. Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS One, 6(9): e24570, https://doi.org/10.1371/journal.pone.0024570.

    Article  Google Scholar 

  85. Zonneveld K A F, Versteegh G J M, Kasten S, Eglinton T I, Emeis K C, Huguet C, Koch B P, de Lange G J, de Leeuw J W, Middelburg J J, Mollenhauer G, Prahl F G, Rethemeyer J, Wakeham S G. 2010. Selective preservation of organic matter in marine environments; processes and impact on the sedimentary record. Biogeosciences, 7(2): 483–511, https://doi.org/10.5194/bg-7-483-2010.

    Article  Google Scholar 

Download references

Acknowledgment

We thank all of the scientists and crew members on-board the R/V Kexue San Hao for the assistance provided in the collection of samples and geochemical data during the cruise.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yu Zhen.

Additional information

Supported by the National Key Research and Development Program of China (No. 2017YFC1404402), the National Natural Science Foundation of China (Nos. 41620104001, 41806131), the Scientific and Technological Innovation Project of the Qingdao National Laboratory for Marine Science and Technology (No. 2016ASKJ02), and the China Postdoctoral Science Foundation (No. 2018M632722)

Data Availability Statement

All data generated and/or analyzed during this study are available from the corresponding author upon request.

Electronic Supplementary Material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chen, Y., Li, S., Xu, X. et al. Characterization of microbial communities in sediments of the South Yellow Sea. J. Ocean. Limnol. (2020). https://doi.org/10.1007/s00343-020-0106-6

Download citation

Keywords

  • microbial community
  • 16S rRNA gene
  • high-throughput sequencing
  • South Yellow Sea
  • sediment