Skip to main content

Advertisement

Log in

Bacterial community structure in intertidal sediments of Fildes Peninsula, maritime Antarctica

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The Fildes Peninsula has a maritime Antarctic climate and has attracted the interest of scientists for decades. The soil bacterial community and the environmental factors shaping it have been well documented. However, the bacterial community of intertidal sediments, which has been determined to play crucial roles in biogeochemical cycles in temperate regions, has been comparatively neglected. Here, the diversity and abundance of bacteria in intertidal sediments represented by 18 samples from the Fildes Peninsula were revealed by 16S rRNA gene pyrosequencing and qPCR. The results showed distinct bacterial community structure, and lower diversity and abundance relative to low-latitude areas. Proteobacteria, Bacteroidetes, and Actinobacteria were the predominant phyla, accounting for ~90 % of the total community. Among the measured environmental factors, chlorophyll a (Chl a), total organic matter (TOM), and standard deviation (σ) of sediment grain size explained the bacterial community variation in the redundancy analysis across all samples, and had consistent relationship with bacterial diversity and abundance. Granulosicoccus, the most abundant genus within Chromatiales Gammaproteobacteria in this study, showed positive correlation with standard deviation of sediment grain size. The present study demonstrated a distinct bacterial community different from temperate regions and provided insights into the potential ecological roles of specific taxa in the Antarctic environment.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH (2013) Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 31:533–538

    Article  CAS  PubMed  Google Scholar 

  • Babalola OO, Kirby BM, Le Roes-Hill M, Cook AE, Cary SC, Burton SG, Cowan DA (2009) Phylogenetic analysis of actinobacterial populations associated with Antarctic Dry Valley mineral soils. Environ Microbiol 11:566–576

    Article  CAS  PubMed  Google Scholar 

  • Boer SI, Hedtkamp SI, van Beusekom JE, Fuhrman JA, Boetius A, Ramette A (2009) Time- and sediment depth-related variations in bacterial diversity and community structure in subtidal sands. ISME J 3:780–791

    Article  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  PubMed Central  Google Scholar 

  • Bowman JP, Cavanagh J, Austin JJ, Sanderson K (1996) Novel Psychrobacter species from Antarctic ornithogenic soils. Int J Syst Bacteriol 46:841–848

    Article  CAS  PubMed  Google Scholar 

  • Bozal N (2003) Characterization of several Psychrobacter strains isolated from Antarctic environments and description of Psychrobacter luti sp. nov. and Psychrobacter fozii sp. nov. Int J Syst Evol Microbiol 53:1093–1100

    Article  CAS  PubMed  Google Scholar 

  • Cameron R, Morelli F, Johnson R (1972) Bacterial species in soil and air of Antarctic continent. Antarct J US 7:187–189

    Google Scholar 

  • Campbell BJ, Kirchman DL (2013) Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J 7:210–220

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8:129–138

    Article  CAS  PubMed  Google Scholar 

  • Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342

    Article  CAS  PubMed  Google Scholar 

  • Chan Y, Van Nostrand JD, Zhou J, Pointing SB, Farrell RL (2013) Functional ecology of an Antarctic dry valley. Proc Natl Acad Sci USA 110:8990–8995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho JC, Giovannoni SJ (2004) Cultivation and growth characteristics of a diverse group of oligotrophic marine gammaproteobacteria. Appl Environ Microbiol 70:432–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christner BC, Priscu JC, Achberger AM et al (2014) A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512:310–313

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunliffe M, Upstill-Goddard RC, Murrell JC (2011) Microbiology of aquatic surface microlayers. FEMS Microbiol Rev 35:233–246

    Article  CAS  PubMed  Google Scholar 

  • Denner EB, Mark B, Busse HJ, Turkiewicz M, Lubitz W (2001) Psychrobacter proteolyticus sp. nov., a psychrotrophic, halotolerant bacterium isolated from the Antarctic krill Euphausia superba Dana, excreting a cold-adapted metalloprotease. Syst Appl Microbiol 24:44–53

    Article  CAS  PubMed  Google Scholar 

  • Deslippe JR, Hartmann M, Simard SW, Mohn WW (2012) Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol Ecol 82:303–315

    Article  CAS  PubMed  Google Scholar 

  • Dinis JM, Barton DE, Ghadiri J et al (2011) In search of an uncultured human-associated TM7 bacterium in the environment. PLoS ONE 6:e21280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan J, Li L, Han J, Ming H, Li J, Na G, Chen J (2013) Diversity and structure of bacterial communities in Fildes Peninsula, King George Island. Polar Biol 36:1385–1399

    Article  Google Scholar 

  • Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Folk RL, Ward WC (1957) Brazos River bar: a study in the significance of grain size parameters. J Sediment Res 27:3–26

    Article  Google Scholar 

  • Foong CP, Wong VLCM, González M (2010) Metagenomic analyses of the dominant bacterial community in the Fildes Peninsula, King George Island (South Shetland Islands). Polar Sci 4:263–273

    Article  Google Scholar 

  • Fortunato CS, Crump BC (2011) Bacterioplankton community variation across river to ocean environmental gradients. FEMS Microbiol Ecol 62:374–382

    Article  Google Scholar 

  • Glöckner F-O, Fuchs BM, Amann RI (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65:3721–3726

    PubMed  PubMed Central  Google Scholar 

  • González J, Fernández-Gómez B, Fernàndez-Guerra A et al (2008) Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proc Natl Acad Sci USA 105:8724–8729

    Article  PubMed  PubMed Central  Google Scholar 

  • Haller L, Poté J, Loizeau JL, Wildi W (2009) Distribution and survival of faecal indicator bacteria in the sediments of the Bay of Vidy, Lake Geneva, Switzerland. Ecol Indic 9:540–547

    Article  Google Scholar 

  • Hang I, Rinttila T, Zentek J, Kettunen A, Alaja S, Apajalahti J, Harmoinen J, de Vos WM, Spillmann T (2012) Effect of high contents of dietary animal-derived protein or carbohydrates on canine faecal microbiota. BMC Vet Res 8:90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He X, McLean J, Edlund A et al (2015) Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle. Proc Natl Acad Sci USA 112:244–249

    Article  CAS  PubMed  Google Scholar 

  • Hughes KA (2003) Influence of seasonal environmental variables on the distribution of presumptive fecal coliforms around an Antarctic research station. Appl Environ Microbiol 69:4884–4891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inman DL (1952) Measures for describing the size distribution of sediments. J Sediment Res 22:125–145

    CAS  Google Scholar 

  • Juni E, Heym GA (1986) Psychrobacter immobilis gen. nov. sp. nov.: genospecies composed of gram-negative, aerobic, oxidase-positive coccobacilli. Int J Syst Evol Microbiol 36:388–391

    Google Scholar 

  • Kampfer P, Albrecht A, Buczolits S, Busse HJ (2002) Psychrobacter faecalis sp. nov., a new species from a bioaerosol originating from pigeon faeces. Syst Appl Microbiol 25:31–36

    Article  CAS  PubMed  Google Scholar 

  • Kennedy AD (1993) Water as a limiting factor in the Antarctic terrestrial environment: a biogeographical synthesis. Arctic Alpine Res 25:308–315

    Article  Google Scholar 

  • Kumar PS, Brooker MR, Dowd SE, Camerlengo T (2011) Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS One 6:e20956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee K, Lee HK, Choi T-H, Kim K-M, Cho J-C (2007) Granulosicoccaceae fam. nov., to include Granulosicoccus antarcticus gen. nov., sp. nov., a non-phototrophic, obligately aerobic chemoheterotroph in the order Chromatiales, isolated from Antarctic seawater. J Microbiol Biotech 17:1483–1490

    CAS  Google Scholar 

  • Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24

    Article  Google Scholar 

  • Liu X-S, Zhang Z-N, Huang Y (2007) Sublittoral meiofauna with particular reference to nematodes in the southern Yellow Sea, China. Estuar Coast Shelf Sci 71:616–628

    Article  Google Scholar 

  • Liu J, Liu X, Wang M, Qiao Y, Zheng Y, Zhang XH (2014) Bacterial and archaeal communities in sediments of the north Chinese marginal seas. FEMS Microbiol Ecol 70:105–117

    Article  Google Scholar 

  • Liu J, Fu B, Yang H, Zhao M, He B, Zhang XH (2015) Phylogenetic shifts of bacterioplankton community composition along the Pearl Estuary: the potential impact of hypoxia and nutrients. Front Microbiol 6:64

    PubMed  PubMed Central  Google Scholar 

  • Lorenzen C, Jeffrey S (1980) Determination of chlorophyll in seawater: report of intercalibration tests. In UNESCO technical papers in Marine Science: UNESCO

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luz AP, Ciapina EMP, Gamba RC, Lauretto MS, Farias EWC, Bicego MC, Taniguchi S, Montone RC, Pellizari VH (2006) Potential for bioremediation of hydrocarbon polluted soils in the Maritime Antarctic. Antarct Sci 18:335–343

    Article  Google Scholar 

  • Martins CC, Rosalinda CM, Gamba RC, Pellizari VH (2005) Sterols and fecal indicator microorganisms in sediments from Admiralty Bay, Antarctica. Braz J Oceanogr 53:1–12

    Article  Google Scholar 

  • McCammon SA, Bowman JP (2000) Taxonomy of Antarctic Flavobacterium species: description of Flavobacterium gillisiae sp. nov., Flavobacterium tegetincola sp. nov., and Flavobacterium xanthum sp. nov., nom. rev. and reclassification of [Flavobacterium] salegens as Salegentibacter salegens gen. nov., comb. nov. Int J Syst Evol Microbiol 50:1055–1063

    Article  CAS  PubMed  Google Scholar 

  • Mudroch A, Azcue JM, Mudroch P (1996) Manual of physico-chemical analysis of aquatic sediments. CRC Press, Frorida

    Google Scholar 

  • Nedashkovskaya OI, Kim SB, Han SK et al (2004) Maribacter gen. nov., a new member of the family Flavobacteriaceae, isolated from marine habitats, containing the species Maribacter sedimenticola sp. nov., Maribacter aquivivus sp. nov., Maribacter orientalis sp. nov. and Maribacter ulvicola sp. nov. Int J Syst Evol Microbiol 54:1017–1023

    Article  CAS  PubMed  Google Scholar 

  • Neufeld JD, Mohn WW (2005) Unexpectedly high bacterial diversity in arctic tundra relative to boreal forest soils, revealed by serial analysis of ribosomal sequence tags. Appl Environ Microbiol 71:5710–5718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunoura T, Takaki Y, Hirai M et al (2015) Hadal biosphere: insight into the microbial ecosystem in the deepest ocean on Earth. Proc Natl Acad Sci USA 112:1230–1236

    Article  Google Scholar 

  • Pan Q, Wang F, Zhang Y, Cai M, He J, Yang H (2013) Denaturing gradient gel electrophoresis fingerprinting of soil bacteria in the vicinity of the Chinese Great Wall Station, King George Island, Antarctica. J Environ Sci 25:1649–1655

    Article  CAS  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596

    Article  Google Scholar 

  • Romanenko LA (2002) Psychrobacter submarinus sp. nov. and Psychrobacter marincola sp. nov., psychrophilic halophiles from marine environments. Int J Syst Evol Microbiol 52:1291–1297

    CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T et al (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  PubMed Central  Google Scholar 

  • Sinkko H, Lukkari K, Sihvonen LM, Sivonen K, Leivuori M, Rantanen M, Paulin L, Lyra C (2013) Bacteria contribute to sediment nutrient release and reflect progressed eutrophication-driven hypoxia in an organic-rich continental sea. PLoS One 8:e67061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith JJ, Tow LA, Stafford W, Cary C, Cowan DA (2006) Bacterial diversity in three different Antarctic Cold Desert mineral soils. Microb Ecol 51:413–421

    Article  PubMed  Google Scholar 

  • Stach JE, Maldonado LA, Masson DG, Ward AC, Goodfellow M, Bull AT (2003) Statistical approaches for estimating actinobacterial diversity in marine sediments. Appl Environ Microbiol 69:6189–6200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka N, Romanenko LA, Iino 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 

  • Teixeira LC, Peixoto RS, Cury JC, Sul WJ, Pellizari VH, Tiedje J, Rosado AS (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J 4:989–1001

    Article  PubMed  Google Scholar 

  • Tischer K, Kleinsteuber S, Schleinitz K et al (2013) Microbial communities along biogeochemical gradients in a hydrocarbon-contaminated aquifer. Environ Microbiol 15:2603–2615

    Article  CAS  PubMed  Google Scholar 

  • Ubeda C, Taur Y, Jenq RR et al (2010) Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest 120:4332–4341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  PubMed Central  Google Scholar 

  • Wang Y, Sheng HF, He Y, Wu JY, Jiang YX, Tam NF, Zhou HW (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl Environ Microbiol 78:8264–8271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Liu L, Zheng B, Zhu Y, Wang X (2013) Analysis of the bacterial community in the two typical intertidal sediments of Bohai Bay, China by pyrosequencing. Mar Pollut Bull 72:181–187

    Article  CAS  PubMed  Google Scholar 

  • Williams KP, Gillespie JJ, Sobral BW, Nordberg EK, Snyder EE, Shallom JM, Dickerman AW (2010) Phylogeny of Gammaproteobacteria. J Bacteriol 192:2305–2314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wulff A, Vilbaste S, Truu J (2005) Depth distribution of photosynthetic pigments and diatoms in the sediments of a microtidal fjord. Hydrobiologia 534:117–130

    Article  CAS  Google Scholar 

  • Wynn-Williams DD (1990) Microbial colonization processes in Antarctic fellfield soil-an experimental overview. Polar Biol 3:164–178

    Google Scholar 

  • Yamamoto N, Lopez G (1985) Bacterial abundance in relation to surface area and organic content of marine sediments. J Exp Mar Biol Ecol 90:209–220

    Article  Google Scholar 

  • Yergeau E, Kowalchuk GA (2008) Responses of Antarctic soil microbial communities and associated functions to temperature and freeze-thaw cycle frequency. Environ Microbiol 10:2223–2235

    Article  PubMed  Google Scholar 

  • Yergeau E, Bokhorst S, Huiskes AH, Boschker HT, Aerts R, Kowalchuk GA (2007a) Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiol Ecol 59:436–451

    Article  CAS  PubMed  Google Scholar 

  • Yergeau E, Kang S, He Z, Zhou J, Kowalchuk GA (2007b) Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J 1:163–179

    Article  CAS  PubMed  Google Scholar 

  • Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007c) Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ Microbiol 9:2670–2682

    Article  CAS  PubMed  Google Scholar 

  • Yergeau E, Schoondermark-Stolk SA, Brodie EL, Dejean S, DeSantis TZ, Goncalves O, Piceno YM, Andersen GL, Kowalchuk GA (2009) Environmental microarray analyses of Antarctic soil microbial communities. ISME J 3:340–351

    Article  CAS  PubMed  Google Scholar 

  • Yergeau E, Bokhorst S, Kang S, Zhou J, Greer CW, Aerts R, Kowalchuk GA (2012) Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. ISME J 6:692–702

    Article  CAS  PubMed  Google Scholar 

  • Yin Q, Fu B, Li B, Shi X, Inagaki F, Zhang XH (2013) Spatial variations in microbial community composition in surface seawater from the ultra-oligotrophic center to rim of the South Pacific Gyre. PLoS One 8:e55148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youssef NH, Elshahed MS (2009) Diversity rankings among bacterial lineages in soil. ISME J 3:305–313

    Article  CAS  PubMed  Google Scholar 

  • Zeng YX, Yu Y, Qiao ZY, Jin HY, Li HR (2014) Diversity of bacterioplankton in coastal seawaters of Fildes Peninsula, King George Island, Antarctica. Arch Microbiol 196:137–147

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Song L, Dong X (2010) Proteiniclasticum ruminis gen. nov., sp. nov., a strictly anaerobic proteolytic bacterium isolated from yak rumen. Int J Syst Evol Microbiol 60:2221–2225

    Article  CAS  PubMed  Google Scholar 

  • Zobell CE (1938) Studies on the bacterial flora of marine bottom sediments. J Sediment Res A 8:10–18

    CAS  Google Scholar 

Download references

Acknowledgments

We thank the Chinese Arctic and Antarctic Administration (CAA), who assisted in the field work. We also would like to express our great appreciation to Prof. Brian Austin (Institute of Aquaculture, University of Stirling, U.K.), who kindly read our paper to improve the English language. This study was supported by the Chinese Polar Environment Comprehensive Investigation and Assessment Program (No. CHINARE2013-02-01 and CHINARE2013-01-06).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiao-Hua Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 345 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Liu, X., Yu, S. et al. Bacterial community structure in intertidal sediments of Fildes Peninsula, maritime Antarctica. Polar Biol 40, 339–349 (2017). https://doi.org/10.1007/s00300-016-1958-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-016-1958-2

Keywords

Navigation