Skip to main content
SpringerLink
Log in

Bacterial and archaeal communities in deep sea waters near the Ninetyeast Ridge in Indian Ocean

  • Ecology
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Depth-dependent distribution patterns of bacterial and archaeal communities in deep sea water column around the Ninetyeast Ridge in the Indian Ocean were investigated using 16S rRNA gene profiling. Sampling was conducted at the northern Ninetyeast Ridge (1°59.89′N–9°59.70′S, 87°58.90′E–88°00.03′E) from September to November 2016 where samples were collected from the bathyal (1 000 m) to bathypelagic depths (>4 000 m) in four different stations. A total of 1 565 405 clean data falling into 6 712 bacterial OTUs and 1 452 727 clean data falling into 806 archaeal OTUs based on 97% similarity level were analyzed. Most of the bacterial 16S rRNA gene sequences were affiliated with Gammaproteobacteria, followed by Alphaproteobacteria and Bacteroidia. The archaeal 16S rRNA gene sequences mostly affiliated to Nitrososphaeria (Thaumarchaeota) dominated with relative abundances ranging from 52.68% to 97.2%, followed by Thermoplasmata (Euryarchaeota). Vertical partitioning of bacterial and archaeal communities among different water layers was observed. Canonical correspondence analysis (CCA) and Spearman’s correlations revealed that depth (P=0.003), dissolved oxygen (P=0.019), and nitrite (P=0.033) were the main environmental factors affecting bacterial community structure at genus level in the Ninetyeast Ridge. On the other hand, the first two CCA axes accounted for 74.4% of the explained total variance, it seems that the archaeal communities at genus level were heavily influenced by the environmental variables including depth, dissolved oxygen (DO), nitrite, salinity, phosphate, ammonia, nitrate, and silicate, but none of them exhibited any significant correlation on the structuring (P>0.1).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data Availability Statement

The original data generated or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • AgoguĂ© H, Lamy D, Neal P R, Sogin M L, Herndl G J. 2011. Water mass-specificity of bacterial communities in the North Atlantic revealed by massively parallel sequencing. Molecular Ecology, 20(2): 258–274.

    Article  Google Scholar 

  • Bandekar M, Ramaiah N, Jain A, Meena R M. 2018. Seasonal and depth-wise variations in bacterial and archaeal groups in the Arabian Sea oxygen minimum zone. Deep Sea Research Part II: Topical Studies in Oceanography, 156: 4–18.

    Article  Google Scholar 

  • Barlett M A, Leff L G. 2010. The effects of N:P ratio and nitrogen form on four major freshwater bacterial taxa in biofilms. Canadian Journal of Microbiology, 56(1): 32–43.

    Article  Google Scholar 

  • Beman J M, Carolan M T. 2013. Deoxygenation alters bacterial diversity and community composition in the ocean’s largest oxygen minimum zone. Nature Communications, 4: 2 705.

    Article  Google Scholar 

  • Biddanda B, Ogdahl M, Cotner J. 2001. Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnology and Oceanography, 46(3): 730–739.

    Article  Google Scholar 

  • Bouvier T C, de Giorgio P A. 2002. Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnology and Oceanography, 47(2): 453–470.

    Article  Google Scholar 

  • Brin L D, Giblin A E, Rich J J. 2014. Environmental controls of anammox and denitrification in Southern New England estuarine and shelf sediments. Limnology and Oceanography, 59(3): 851–860.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Chao A, Ma M-C, Yang M C K. 1993. Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika, 80(1): 193–201.

    Article  Google Scholar 

  • Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11(4): 265–270.

    Google Scholar 

  • Cho J C C, Giovannoni S J. 2004. Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Applied and Environmental Microbiology, 70(1): 432–440.

    Article  Google Scholar 

  • Christner B C, Priscu J C, Achberger AM, Barbante C, Carter S P, Christianson K, Michaud A B, Mikucki J A, Mitchell A C, Skidmore M L, Vick-Majors T J, the WISSARD Science Team. 2014. A microbial ecosystem beneath the West Antarctic ice sheet. Nature, 512(7514): 310–313.

    Article  Google Scholar 

  • Cottrell M T, Waidner L A, Yu L Y, Kirchman D L. 2005. Bacterial diversity of metagenomic and PCR libraries from the Delaware River. Environmental Microbiology, 7(12): 1 883–1 895.

    Article  Google Scholar 

  • Cunliffe M, Upstill-Goddard R C, Murrell J C. 2011. Microbiology of aquatic surface microlayers. FEMS Microbiology Reviews, 35(2): 233–246.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16): 2 194–2 200.

    Article  Google Scholar 

  • Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996–998.

    Article  Google Scholar 

  • Feng B W, Li X R, Wang J H, Hu Z Y, Meng H, Xiang L Y, Quan Z X. 2009. Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiology Ecology, 70(2): 236–248.

    Article  Google Scholar 

  • Freedman Z, Zak D R. 2014. Atmospheric N deposition increases bacterial laccase-like multicopper oxidases: implications for organic matter decay. Applied and Environmental Microbiology, 80(14): 4 460–4 468.

    Article  Google Scholar 

  • Guo X P, Lu D P, Niu Z S, Feng J N, Chen Y R, Tou F Y, Liu M, Yang Y. 2018. Bacterial community structure in response to environmental impacts in the intertidal sediments along the Yangtze Estuary, China. Marine Pollution Bulletin, 126: 141–149.

    Article  Google Scholar 

  • Guo X P, Niu Z S, Lu D P, Feng J N, Chen Y R, Tou F Y, Liu M, Yang Y. 2017. Bacterial community structure in the intertidal biofilm along the Yangtze estuary, China. Marine Pollution Bulletin, 124(1): 314–320.

    Article  Google Scholar 

  • Haas B J, Gevers D, Earl A M, Feldgarden M, Ward D V, Giannoukos G, Ciulla D, Tabbaa D, Highlander S K, Sodergren E, MethĂ© B, DeSantis T Z, Human Microbiome Consortium, 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.

    Article  Google Scholar 

  • Haggerty J M, Dinsdale E A. 2017. Distinct biogeographical patterns of marine bacterial taxonomy and functional genes. Global Ecology and Biogeography, 26(2): 177–190.

    Article  Google Scholar 

  • Han D, Ha H K, Hwang C Y, Lee B Y, Hur H G, Lee Y K. 2015. Bacterial communities along stratified water columns at the Chukchi Borderland in the western Arctic Ocean. Deep Sea Research Part II: Topical Studies in Oceanography, 120: 52–60.

    Article  Google Scholar 

  • Hugoni M, Domaizon I, Taib N, Biderre-Petit C, AgoguĂ© H, Galand P E, Debroas D, Mary I. 2015. Temporal dynamics of active Archaea in oxygen-depleted zones of two deep lakes. Environmental Microbiology Reports, 7(2): 321–329.

    Article  Google Scholar 

  • Jamieson R E, Heywood J L, Rogers A D, Billett D S M, Pearce D A. 2013. Bacterial biodiversity in deep-sea sediments from two regions of contrasting surface water productivity near the Crozet Islands, Southern Ocean. Deep Sea Research Part I: Oceanographic Research Papers, 75: 67–77.

    Article  Google Scholar 

  • Kirchman D L. 2016. Growth rates of microbes in the oceans. Annual Review of Marine Science, 8: 285–309.

    Article  Google Scholar 

  • Könneke M, Bernhard A E, de la Torre J R, Walker C B, Waterbury J B, Stahl D A. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437(7058): 543–546.

    Article  Google Scholar 

  • Könneke M, Lipp S J, Hinrichs K U. 2012. Carbon isotope fractionation by the marine ammonia-oxidizing archaeon Nitrosopumilus maritimus. Organic Geochemistry, 48(7): 21–24.

    Article  Google Scholar 

  • Krishna K S, Rao D G, Raju L V S, Chaubey A K, Shcherbakov V S, Pilipenko A I, Murthy I V R. 1999. Paleocene on-spreading-axis hotspot volcanism along the Ninetyeast Ridge: an interaction between the Kerguelen hotspot and the Wharton spreading center. Proceedings of the Indian Academy of Sciences—Earth and Planetary Sciences, 108(4): 255–267.

    Google Scholar 

  • Kruskal J B. 1964. Nonmetric multidimensional scaling: A numerical method. Psychometrika, 29(2): 115–129.

    Article  Google Scholar 

  • Kumar R, Mishra A, Jha B. 2019. Bacterial community structure and functional diversity in subsurface seawater from the western coastal ecosystem of the Arabian Sea, India. Gene, 701: 55–64.

    Article  Google Scholar 

  • Kumar S P, Narvekar J, Nuncio M, Gauns M, Sardesai S. 2009. What drives the biological productivity of the northern Indian Ocean? In: Wiggert J D, Hood R R, Naqvi S W A, Brink K H, Smith S L eds. Indian Ocean Biogeochemical Processes and Ecological Variability, Volume 185. Washington: American Geophysical Union.

    Google Scholar 

  • Li J L, Li N, Li F C, Zou T, Yu S X, Wang Y C, Qin S, Wang G Y. 2014. Spatial diversity of bacterioplankton communities in surface water of northern South China Sea. PLoS One, 9(11): e113014.

    Article  Google Scholar 

  • Li Y J, Xu L Y. 2007. Improvement for unweighted pair group method with arithmetic mean and its application. Journal of Beijing University of Technology, 33(12): 1 333–1 339. (in Chinese with English abstract)

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Liu J W, Liu X S, Wang M, Qiao Y L, Zheng Y F, Zhang X H. 2015. Bacterial and archaeal communities in sediments of the North Chinese marginal seas. Microbial Ecology, 70(1): 105–117.

    Article  Google Scholar 

  • Liu J W, Zheng Y F, Lin H Y, Wang X C, Li M, Liu Y, Yu M, Zhao M X, Pedentchouk N, Lea-Smith D J, Todd J D, Magill C R, Zhang W J, Zhou S, Song D L, Zhong H H, Xin Y, Yu M, Tian J W, Zhang X H. 2019. Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench. Microbiome, 7: 47.

    Article  Google Scholar 

  • Martens-Habbena W, Berube P M, Urakawa H, de la Torre J R, Stahl D A. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature, 461(7266): 976–979.

    Article  Google Scholar 

  • Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. Journal, 17(1): 10–12.

    Article  Google Scholar 

  • McArthur J V. 2013. Processes in Microbial Ecology by David L. Kirchman. Quarterly Review of Biology, 88(2): 143–144.

    Article  Google Scholar 

  • Menezes L D, Fernandes G L, Mulla A B, Meena R M, Damare S R. 2018. Diversity of culturable sulphur-oxidising bacteria in the oxygen minimum zones of the northern Indian Ocean. Journal of Marine Systems, https://doi.org/10.1016/j.jmarsys.2018.05.007.

  • Michael L, Krishna K S. 2011. Dating of the 85°E Ridge (northeastern Indian Ocean) using marine magnetic anomalies. Current Science, 100(9): 1 314–1 322.

    Google Scholar 

  • Michelsen C F, Pedas P, Glaring M A, Schjoerring J K, Stougaard P. 2013. Bacterial diversity in Greenlandic soils as affected by potato cropping and inorganic versus organic fertilization. Polar Biology, 37(1): 61–71.

    Article  Google Scholar 

  • Naqvi S W A. 2006. Oxygen deficiency in the North Indian Ocean. Gayana, 70(S1): 53–58.

    Google Scholar 

  • Offre P, Spang A, Schleper C. 2013. Archaea in biogeochemical cycles. Annual Review of Microbiology, 67: 437–457.

    Article  Google Scholar 

  • Parsons T R, Maita Y, Lalli C M. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, UK.

    Google Scholar 

  • Paulmier A, Ruiz-Pino D. 2009. Oxygen minimum zones (OMZs) in the modern ocean. Progress in Oceanography, 80(3–4): 113–128.

    Article  Google Scholar 

  • Qian G, Wang J, Kan J J, Zhang X D, Xia Z Q, Zhang X C, Miao Y Y, Sun J. 2018. Diversity and distribution of anammox bacteria in water column and sediments of the Eastern Indian Ocean. International Biodeterioration & Biodegradation, 133: 52–62.

    Article  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner F O. 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1): D590–D596.

    Article  Google Scholar 

  • Rysgaard S, Glud R N, Risgaard-Petersen N, Dalsgaard T. 2004. Denitrification and anammox activity in arctic marine sediments. Limnology and Oceanography, 49(5): 1 493–1 502.

    Article  Google Scholar 

  • Sheik C S, Mitchell T W, Rizvi F Z, Rehman Y, Faisal M, Hasnain S, McInerney M J, Krumholz L R. 2012. Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PLoS One, 7(6): e40059.

    Article  Google Scholar 

  • Shulse C N, Maillot B, Smith C R, Church M J. 2017. Polymetallic nodules, sediments, and deep waters in the equatorial North Pacific exhibit highly diverse and distinct bacterial, archaeal, and microeukaryotic communities. Microbiology, 6(2): e00428.

    Article  Google Scholar 

  • Sogin M L, Morrison H G, Huber J A, Mark Welch D, Huse S M, Neal P R, Arrieta J M, Herndl G J. 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences of the United States of America, 103(32): 12 115–12 120.

    Article  Google Scholar 

  • Stahl D A, de la Torre J R. 2012. Physiology and diversity of ammonia-oxidizing Archaea. Annual Review of Microbiology, 66: 83–101.

    Article  Google Scholar 

  • Terahara T, Yamada K, Nakayama J, Igarashi Y, Kobayashi T, Imada C. 2016. Bacterial community structures of deep-sea water investigated by molecular biological techniques. Gene, 576(2): 696–700.

    Article  Google Scholar 

  • Williams T J, Wilkins D, Long E, Evans F, DeMaere M Z, Raftery M J, Ricardo C. 2013. The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environmental Microbiology, 15(5): 1 302–1 317.

    Article  Google Scholar 

  • Xie L S, Xu L, He Y, Zhang Y, Wang J H, Xu J. 2017. Archaeal diversity in the euphotic seawater at a slope in the northern South China Sea. Chinese Journal of Applied & Environmental Biology, 23(1): 22–27. (in Chinese with English abstract)

    Google Scholar 

  • Zhang L K, Kang M Y, Xu J J, Xu J, Shuai Y J, Zhou X J, Yang Z H, Ma K S. 2016. Bacterial and archaeal communities in the deep-sea sediments of inactive hydrothermal vents in the Southwest India Ridge. Scientific Reports, 6: 25 982.

    Article  Google Scholar 

  • Zheng Y L, Hou L J, Newell S, Liu M, Zhou J L, Zhao H, You L L, Cheng X L. 2014. Community dynamics and activity of ammonia-oxidizing prokaryotes in intertidal sediments of the Yangtze estuary. Applied and Environmental Microbiology, 80(1): 408–419.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources (MNR), Qingdao, 266061, China

    Ping Gao, Lingyun Qu, Guangxun Du, Qinsheng Wei, Xuelei Zhang & Guang Yang

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Ping Gao & Lingyun Qu

  3. Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Qinsheng Wei

Authors
  1. Ping Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lingyun Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guangxun Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qinsheng Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xuelei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lingyun Qu.

Additional information

Supported by the China Ocean Mineral Resources Research and Development Association Program (Nos. DY135-E2-1-01, DY135-E2-4-00), the China Global Sea-Atmosphere Interaction Research Program (No. GASI-02-IND-STSsum), and the S&T Innovation Project of Qingdao National Laboratory for Marine Science and Technology (No. 2016ASKJ14)

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, P., Qu, L., Du, G. et al. Bacterial and archaeal communities in deep sea waters near the Ninetyeast Ridge in Indian Ocean. J. Ocean. Limnol. 39, 582–597 (2021). https://doi.org/10.1007/s00343-020-9343-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-020-9343-y

Keyword

Search

Navigation