Skip to main content

Advertisement

SpringerLink
Log in

Diversity of bacterioplankton in coastal seawaters of Fildes Peninsula, King George Island, Antarctica

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The bacterioplankton not only serves critical functions in marine nutrient cycles, but can also serve as indicators of the marine environment. The compositions of bacterial communities in the surface seawater of Ardley Cove and Great Wall Cove were analyzed using a 16S rRNA multiplex 454 pyrosequencing approach. Similar patterns of bacterial composition were found between the two coves, in which Bacteroidetes, Alphaproteobacteria, and Gammaproteobacteria were the dominant members of the bacterioplankton communities. In addition, a large fraction of the bacterial sequence reads (on average 5.3 % per station) could not be assigned below the domain level. Compared with Ardley Cove, Great Wall Cove showed higher chlorophyll and particulate organic carbon concentrations and exhibited relatively lower bacterial richness and diversity. Inferred metabolisms of summer bacterioplankton in the two coves were characterized by chemoheterotrophy and photoheterotrophy. Results suggest that some cosmopolitan species (e.g., Polaribacter and Sulfitobacter) belonging to a few bacterial groups that usually dominate in marine bacterioplankton communities may have similar ecological functions in similar marine environments but at different geographic locations.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bano N, Hollibaugh JT (2000) Diversity and distribution of DNA sequences with affinity to ammonia-oxidizing bacteria of the β subdivision of the class Proteobacteria in the Arctic Ocean. Appl Environ Microbiol 66:1960–1969

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Biebl H, Wagner-Döbler I (2006) Growth and bacteriochlorophyll a formation in taxonomically diverse aerobic anoxygenic phototrophic bacteria in chemostat culture: influence of light regimen and starvation. Process Biochem 41:2153–2159

    Article  CAS  Google Scholar 

  • Boeuf D, Cottrell MT, Kirchman DL, Lebaron P, Jeanthon C (2013) Summer community structure of aerobic anoxygenic phototrophic bacteria in the western Arctic Ocean. FEMS Microbiol Ecol 85:417–432

    Article  CAS  PubMed  Google Scholar 

  • Bolhuis H, Stal LJ (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME J 5:1701–1712

    Article  CAS  PubMed  Google Scholar 

  • Bosshard PP, Santini Y, Grüter DG, Stettler R, Bachofen R (2000) Bacterial diversity and community composition in the chemocline of the meromictic alpine Lake Cadagno as revealed by 16S rRNA gene analysis. FEMS Microbiol Ecol 31:173–182

    Article  CAS  PubMed  Google Scholar 

  • Bowman JS, Rasmussen S, Blom N, Deming JW, Rysgaard S, Sicheritz-Ponten T (2012) Microbial community structure of Arctic multiyear sea ice and surface seawater by 454 sequencing of the 16S RNA gene. ISME J 6:11–20

    Article  CAS  PubMed  Google Scholar 

  • Brown MV, Bowman JP (2001) A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol Ecol 35:267–275

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522

    Article  CAS  PubMed  Google Scholar 

  • Chen JS, Toth J, Kasap M (2001) Nitrogen-fixation genes and nitrogenase activity in Clostridium acetobutylicum and Clostridium beijerinckii. J Ind Microbiol Biotechnol 27:281–286

    Article  PubMed  Google Scholar 

  • Cottrell MT, Kirchman DL (2000a) Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Appl Environ Microbiol 66:5116–5122

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cottrell MT, Kirchman DL (2000b) Natural assemblages of marine Proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66:1692–1697

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Curson AR, Rogers R, Todd JD, Brearley CA, Johnston AW (2008) Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine alpha-proteobacteria and Rhodobacter sphaeroides. Environ Microbiol 10:757–767

    Article  CAS  PubMed  Google Scholar 

  • Darcy JL, Lynch RC, King AJ, Robeson MS, Schmidt SK (2011) Global distribution of Polaromonas phylotypes—evidence for a highly successful dispersal capacity. PLoS ONE 6:e23742

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ducklow HW (2000) Bacterial production and biomass in the oceans. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 85–120

    Google Scholar 

  • Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59

    Article  CAS  Google Scholar 

  • Ghiglione JF, Murray AE (2012) Pronounced summer to winter differences and higher wintertime richness in coastal Antarctic marine bacterioplankton. Environ Microbiol 14:617–629

    Article  CAS  PubMed  Google Scholar 

  • Ghiglione JF, Galand PE, Pommier T, Pedrós-Alió C, Maas EW, Bakker K, Bertilson S, Kirchmanj DL, Lovejoy C, Yager PL, Murray AE (2012) Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc Natl Acad Sci USA 109:17633–17638

    Article  CAS  PubMed  Google Scholar 

  • Giovannoni SJ, Rappé M (2000) Evolution, diversity and molecular ecology of marine prokaryotes. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 47–84

    Google Scholar 

  • Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Environ Microbiol 66:5053–5065

    Article  PubMed Central  PubMed  Google Scholar 

  • González JM, Kiene RP, Moran MA (1999) Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Appl Environ Microbiol 65:3810–3819

    PubMed Central  PubMed  Google Scholar 

  • González JM, Fernández-Gómez B, Fernàndez-Guerra A, Gómez-Consarnau L, Sánchez O, Coll-Lladó M, Del Campo J, Escudero L, Rodríguez-Martínez R, Alonso-Sáez L, Latasa M, Paulsen I, Nedashkovskaya O, Lekunberri I, Pinhassi J, Pedrós-Alió C (2008) Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED 152 (Flavobacteria). Proc Natl Acad Sci USA 105:8724–8729

    Article  PubMed  Google Scholar 

  • Granéli W, Carlsson P, Bertilsson S (2004) Bacterial abundance, production and organic carbon limitation in the Southern Ocean (39–62°S, 4–14°E) during the austral summer 1997/1998. Deep Sea Res II 51:2569–2582

    Article  Google Scholar 

  • Grzymski JJ, Riesenfeld CS, Williams TJ, Dussaq AM, Ducklow H, Erickson M, Cavicchioli R, Murray AE (2012) A metagenomic assessment of winter and summer bacterioplankton from Antarctica Peninsula coastal surface waters. ISME J 6:1901–1915

    Article  CAS  PubMed  Google Scholar 

  • Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis. Wiley-VCH, Weinheim, pp 191–228

    Google Scholar 

  • Huber JA, Welch DBM, Morrison HG, Huse SM, Neal PR, Butterfield DA, Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318:97–100

    Article  CAS  PubMed  Google Scholar 

  • Ilinskiy VV, Gorshkov AN (2004) Free-living and associated bacteria in the coastal waters of Ardley Cove (King George Island, Antarctica): quantitative change from February to October. Polarforschung 72:31–40

    Google Scholar 

  • Jamieson RE, Rogers AD, Billett DS, Smale DA, Pearce DA (2012) Patterns of marine bacterioplankton biodiversity in the surface waters of the Scotia Arc, Southern Ocean. FEMS Microbiol Ecol 80:452–468

    Article  CAS  PubMed  Google Scholar 

  • Kurilenko VV, Christen R, Zhukova NV, Kalinovskaya NI, Mikhailov VV, Crawford RJ, Ivanova EP (2010) Granulosicoccus coccoides sp. nov., isolated from leaves of seagrass (Zostera marina). Int J Syst Evol Microbiol 60:972–976

    Article  PubMed  Google Scholar 

  • Legendre L, Ackley SF, Dieckmann GS, Gulliksen B, Horner R, Hoshiai T, Melnikov IA, Roburgh WS, Spindler M, Sullivan CW (1992) Ecology of sea ice biota. Polar Biol 12:429–444

    Google Scholar 

  • Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120

    Article  PubMed Central  PubMed  Google Scholar 

  • Ma Y, Zhang F, Yang H, Lin L, He J (2013) Detection of phytoplankton blooms at Antarctic coastal water, with an online mooring system during summer 2010/2011. Antarct Sci. doi:10.1017/S0954102013000400

    Google Scholar 

  • Moran MA, Belas R, Schell MA, González JM, Sun F, Sun S, Binder BJ, Edmonds J, Ye W, Orcutt B, Howard EC, Meile C, Palefsky W, Goesmann A, Ren Q, Paulsen I, Ulrich LE, Thompson LS, Saunders E, Buchan A (2007) Ecological genomics of marine Roseobacters. Appl Environ Microbiol 73:4559–4569

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mou X, Moran MA, Stepanauskas R, González JM, Hodson RE (2005) Flow-cytometric cell sorting and subsequent molecular analyses for culture-independent identification of bacterioplankton involved in dimethylsulfoniopropionate transformations. Appl Environ Microbiol 71:1405–1416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park JR, Bae JW, Nam YD, Chang HW, Kwon HY, Quan ZX, Park YH (2007) Sulfitobacter litoralis sp. nov., a marine bacterium isolated from the East Sea, Korea. Int J Syst Evol Microbiol 57:692–695

    Article  CAS  PubMed  Google Scholar 

  • Pinhassi J, Winding A, Binnerup SJ, Zweifel UL, Riemann B, Hagström Å (2003) Spatial variability in bacterioplankton community composition at the Skagerrak-Kattegat front. Mar Ecol Prog Ser 255:1–13

    Article  CAS  Google Scholar 

  • Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrasé C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  • Prabagaran SR, Manorama R, Delille D, Shivaji S (2007) Predominance of Roseobacter, Sulfitobacter, Glaciecola and Psychrobacter in seawater collected off Ushuaia, Argentina, Sub-Antarctica. FEMS Microbiol Ecol 59:342–355

    Article  CAS  PubMed  Google Scholar 

  • Rappé MS, Vergin K, Giovannoni SJ (2000) Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiol Ecol 33:219–232

    Article  PubMed  Google Scholar 

  • Riemann L, Leitet C, Pommier T, Simu K, Holmfeldt K, Larsson U, Hagström A (2008) The native bacterioplankton community in the central Baltic Sea is influenced by freshwater bacterial species. Appl Environ Microbiol 74:503–515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Romanenko LA, Tanaka N, Frolova GM, Mikhailov VV (2010) Arenicella xantha gen. nov., sp. nov., a gammaproteobacterium isolated from a marine sandy sediment. Int J Syst Evol Microbiol 60:1832–1836

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci USA 103:12115–12120

    Article  CAS  PubMed  Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Fish Res Board Can Bulletin 167:311

    Google Scholar 

  • Tada Y, Taniguchi A, Nagao I, Miki T, Uematsu M, Tsuda A, Hamasaki K (2011) Differing growth responses of major phylogenetic groups of marine bacteria to natural phytoplankton blooms in the Western North Pacific Ocean. Appl Environ Microbiol 77:4055–4065

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanaka N, Romanenko LA, Lino T, Frolova GM, Mikhailov VV (2011) Cocleimonas flava gen. nov., sp. nov., a gammaproteobacterium isolated from sand snail (Umbonium costatum). Int J Syst Evol Microbiol 61:412–416

    Article  CAS  PubMed  Google Scholar 

  • Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glöckner FO, Schweder T, Amann R (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611

    Article  CAS  PubMed  Google Scholar 

  • ter Braak CJF, Šmilauer P (2002) Canoco reference manual and CanoDraw for Windows user’s guide: software for Canonical Community Ordination (Version 4.5). Microcomputer Power, Ithaca

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yakimov MM, Gentile G, Bruni V, Cappello S, D’Auria G, Golyshin PN, Giuliano L (2004) Crude oil-induced structural shift of coastal bacterial communities of rod bay (Terra Nova Bay, Ross Sea, Antarctica) and characterization of cultured cold-adapted hydrocarbonoclastic bacteria. FEMS Microbiol Ecol 49:419–432

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Zhu M, Li R, Xia B, Huang F (1999) The phytoplankton in the Antarctic Great Wall Bay in summer. Chin J Polar Res 11(1):42–48 (In Chinese)

    Google Scholar 

  • Zeng YX, Zhang F, He JF, Lee SH, Qiao ZY, Yu Y, Li HR (2013) Bacterioplankton community structure in the Arctic waters as revealed by pyrosequencing of 16S rRNA genes. Antonie Van Leeuwenhoek 103:1309–1319

    Article  PubMed  Google Scholar 

  • Zwart G, Crump BC, Kamst-van Agterveld MP, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155

    Article  Google Scholar 

Download references

Acknowledgments

We appreciate the assistance of the Chinese Arctic and Antarctic Administration who organized the 28th Chinese National Antarctic Research Expedition. This work was supported by the National Natural Science Foundation of China (Grant No. 41076131), Chinese Polar Environment Comprehensive Investigation and Assessment Program (CHINARE2014-02-01, CHINARE2014-04-01), and National High-Tech Research and Development Program of China (Grant No. 2012AA021706).

Author information

Authors and Affiliations

  1. Key Laboratory for Polar Science of State Oceanic Administration, Polar Research Institute of China, Shanghai, 200136, China

    Yin-Xin Zeng, Yong Yu, Zong-Yun Qiao & Hui-Rong Li

  2. College of Biological Engineering, Jimei University, Xiamen, 361021, China

    Yin-Xin Zeng & Zong-Yun Qiao

  3. Laboratory of Marine Ecosystem and Biogeochemistry of State Oceanic Administration, Second Institute of Oceanography, Hangzhou, 310012, China

    Hai-Yan Jin

Authors
  1. Yin-Xin Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zong-Yun Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hai-Yan Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hui-Rong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yin-Xin Zeng.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeng, YX., Yu, Y., Qiao, ZY. et al. Diversity of bacterioplankton in coastal seawaters of Fildes Peninsula, King George Island, Antarctica. Arch Microbiol 196, 137–147 (2014). https://doi.org/10.1007/s00203-013-0950-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-013-0950-2

Keywords

Search

Navigation