Skip to main content

Advertisement

SpringerLink
Log in

Wind-driven distribution of bacteria in coastal Antarctica: evidence from the Ross Sea region

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

Abstract

Wind is a major transporter of biotic and abiotic material in coastal Antarctica. Sulfate-depleted sea salts delivered by wind to the Antarctic interior are thought to derive from sea ice, signifying a connection between Antarctic coastal environments and the interior. We hypothesized that bacteria, known to concentrate in salt-rich environments on the surface of sea ice, may also be subject to wind-driven transport. To test this hypothesis, we undertook a comparative evaluation of the composition and structure of bacterial communities, determined by deep sequencing of the V4 region of the 16S rRNA gene, in samples of frost flowers, young sea ice, and seawater from two coastal sites north of Ross Island, Antarctica, and in fresh snow over land and in surface ice of the Wilson Piedmont and Taylor Glaciers. Contrary to expectation, sequence reads that were consistently found in frost flowers, presumed to be the most mobile element of the sea ice environment, were rarely found in the terrestrial samples. Instead, cyanobacterial reads associated with the genus Pseudanabaena and found in abundance in the glacial ice and snow samples comprised up to 14.1 % of frost flower communities at one of our sites. Although this clade had not previously been reported in the Ross Sea region, wind patterns and other published data suggest that a likely source may be terrestrial aquatic environments on nearby Ross Island, including Mt. Erebus. One member of a sulfur-oxidizing, halophilic clade of the Gammaproteobacteria previously associated with hydrothermal sites was more abundant in frost flowers than in any other sample type. We hypothesize that these bacteria originated from hydrothermally influenced environments on Mt. Erebus. Overall, these findings suggest that wind is an important mechanism of microbial transport between the terrestrial and marine environments in coastal Antarctica, and may facilitate the exchange of taxa and genetic material between isolated habitats.

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

  • Alonso-Sáez L, Galand PE, Casamayor EO, Pedrós-Alió C, Bertilsson S (2010) High bicarbonate assimilation in the dark by Arctic bacteria. ISME J 4:1581–1590. doi:10.1038/ismej.2010.69

    Article  PubMed  Google Scholar 

  • Atkins CB, Dunbar GB (2009) Aeolian sediment flux from sea ice into Southern McMurdo Sound, Antarctica. Glob Planet Change 69:133–141. doi:10.1016/j.gloplacha.2009.04.006

    Article  Google Scholar 

  • Austin DA, Moss MO (1986) Numerical taxonomy of red-pigmented bacteria isolated from a lowland river, with the description of a new taxon, Rugamonas rubra gen. nov., sp. nov. Microbiology 132:1899–1909. doi:10.1099/00221287-132-7-1899

    Article  CAS  Google Scholar 

  • Barber DG, Ehn JK, Pućko M, Rysgaard S, Deming JW, Bowman JS, Papakyriakou T, Galley RJ, Søgaard DH (2014) Frost flowers on young Arctic sea ice: the climatic, chemical and microbial significance of an emerging ice type. J Geophys Res Atmos 119:11593–11612. doi:10.1002/2014JD021736

    Article  CAS  Google Scholar 

  • Beaudon E, Moore J (2009) Frost flower chemical signature in winter snow on Vestfonna ice cap (Nordaustlandet, Svalbard). Cryosphere Discuss 3:159–180. doi:10.5194/tcd-3-159-2009

    Article  Google Scholar 

  • Berger SA, Krompass D, Stamatakis A (2011) Performance, accuracy, and web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol 60:291–302. doi:10.1093/sysbio/syr010

    Article  PubMed  PubMed Central  Google Scholar 

  • Bottos EM, Woo AC, Zawar-Reza P, Pointing SB, Cary SC (2014) Airborne bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica. Microb Ecol 67:120–128. doi:10.1007/s00248-013-0296-y

    Article  PubMed  Google Scholar 

  • Bowman JS, Deming JW (2010) Elevated bacterial abundance and exopolymers in saline frost flowers and implications for atmospheric chemistry and microbial dispersal. Geophys Res Lett 37:1–5. doi:10.1029/2010GL043020

    Article  Google Scholar 

  • Bowman JS, Ducklow HW (2015) Microbial communities can be described by metabolic structure: a general framework and application to a seasonally variable, depth-stratified microbial community from the coastal West Antarctic Peninsula. PLoS One 10:e0135868. doi:10.1371/journal.pone.0135868

    Article  PubMed  PubMed Central  Google Scholar 

  • Bowman JS, Larose C, Vogel TM, Deming JW (2013) Selective occurrence of Rhizobiales in frost flowers on the surface of young sea ice near Barrow, Alaska and distribution in the polar marine rare biosphere. Environ Microbiol Rep 5:575–582. doi:10.1111/1758-2229.12047

    Article  CAS  PubMed  Google Scholar 

  • Bowman JS, Berthiaume CT, Armbrust EV, Deming JW (2014) The genetic potential for key biogeochemical processes in Arctic frost flowers and young sea ice revealed by metagenomic analysis. FEMS Microbiol Ecol 89:376–387. doi:10.1111/1574-6941.12331

    Article  CAS  PubMed  Google Scholar 

  • Breezee J, Cady N, Staley JT (2004) Subfreezing growth of the sea ice bacterium Psychromonas ingrahamii. Microb Ecol 47:300–304. doi:10.1007/s00248-003-1040-9

    Article  CAS  PubMed  Google Scholar 

  • Broady PA, Kibblewhite AL (1991) Morphological characterization of Oscillatoriales (Cyanobacteria) from Ross Island and southern Victoria Land, Antarctica. Antarct Sci 3:35–45. doi:10.1017/S095410209100007X

    Article  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. doi:10.1073/pnas.1000080107

    PubMed Central  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi:10.1038/ismej.2012.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35:169–172. doi:10.1093/nar/gkl889

    Article  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform 11:485. doi:10.1186/1471-2105-11-485

    Article  Google Scholar 

  • de los Ríos A, Ascaso C, Wierzchos J, Fernández-valiente E, Quesada A (2004) Microstructural characterization of cyanobacterial mats from the McMurdo Ice Shelf, Antarctica. Appl Environ Microb 70:569–580. doi:10.1128/AEM.70.1.569

    Article  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microb 72:5069–5072. doi:10.1128/AEM.03006-05

    Article  CAS  Google Scholar 

  • Douglas TA, Domine F, Barret M, Anastasio C, Beine HJ, Bottenheim J, Grannas A, Houdier S, Netcheva S, Rowland G, Staebler R, Steffen A (2012) Frost flowers growing in the Arctic ocean–atmosphere–sea ice–snow interface: 1. Chemical composition. J Geophys Res 117:1–15. doi:10.1029/2011JD016460

    Google Scholar 

  • Eronen-Rasimus E, Kaartokallio H, Lyra C, Autio R, Kuosa H, Dieckmann GS, Thomas DN (2014) Bacterial community dynamics and activity in relation to dissolved organic matter availability during sea-ice formation in a mesocosm experiment. MicrobiologyOpen 3:139–156. doi:10.1002/mbo3.157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ewert M, Carpenter SD, Colangelo-Lillis J, Deming JW (2013) Bacterial and extracellular polysaccharide content of brine-wetted snow over Arctic winter first-year sea ice. J Geophys Res Ocean 118:726–735. doi:10.1002/jgrc.20055

    Article  CAS  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. doi:10.1038/ismej.2012.31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han MV, Zmasek CM (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinform 10:356. doi:10.1186/1471-2105-10-356

    Article  Google Scholar 

  • Herbold CW, Lee CK, McDonald IR, Cary SC (2014) Evidence of global-scale aeolian dispersal and endemism in isolated geothermal microbial communities of Antarctica. Nat Commun 5:3875. doi:10.1038/ncomms4875

    Article  CAS  PubMed  Google Scholar 

  • Hughes KA, McCartney HA, Lachlan-Cope TA, Pearce DA (2004) A preliminary study of airborne microbial biodiversity over Peninsular Antarctica. Cell Mol Biol 50:537–542

    CAS  PubMed  Google Scholar 

  • Jungblut A, Hawes I, Mountfort D, Hitzfeld B, Dietrich DR, Burns BP, Neilan BA (2005) Diversity within cyanobacterial mat communities in variable salinity meltwater ponds of McMurdo Ice Shelf, Antarctica. Environ Microbiol 7:519–529. doi:10.1111/j.1462-2920.2004.00717.x

    Article  CAS  PubMed  Google Scholar 

  • Kellogg CTE, Deming JW (2009) Comparison of free-living, suspended particle, and aggregate-associated Bacterial and Archaeal communities in the Laptev Sea. Aquat Microb Ecol 57:1–18. doi:10.3354/ame01317

    Article  Google Scholar 

  • Kim J-G, Park S-J, Quan Z-X, Jung M-Y, Cha I-T, Kim S-J, Kim K-H, Yang E-J, Kim Y-N, Lee S-H, Rhee S-K (2013) Unveiling abundance and distribution of planktonic Bacteria and Archaea in a polynya in Amundsen Sea, Antarctica. Environ Microbiol 16:1566–1578. doi:10.1111/1462-2920.12287

    Article  PubMed  Google Scholar 

  • Luria C, Ducklow H, Amaral-Zettler L (2014) Marine Bacterial, Archaeal and Eukaryotic diversity and community structure on the continental shelf of the western Antarctic Peninsula. Aquat Microb Ecol 73:107–121. doi:10.3354/ame01703

    Article  Google Scholar 

  • Marion GM, Farren RE, Komrowski AJ (1999) Alternative pathways for seawater freezing. Cold Reg Sci Technol 29:259–266. doi:10.1016/S0165-232X(99)00033-6

    Article  Google Scholar 

  • Marshall KT, Morris RM (2013) Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade. ISME J 7:452–455. doi:10.1038/ismej.2012.78

    Article  CAS  PubMed  Google Scholar 

  • Matsen FA, Kodner RB, Armbrust EV (2010) pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform 11:538. doi:10.1186/1471-2105-11-538

    Article  Google Scholar 

  • Michaud AB, Marie S, Priscu JC (2012) Cyanobacterial diversity across landscape units in a polar desert: Taylor Valley, Antarctica. FEMS Microb Ecol 82:268–278. doi:10.1111/j.1574-6941.2012.01297.x

    Article  CAS  Google Scholar 

  • Miller LA, Fripiat F, Else BGT, Bowman JS, Brown KA, Collins RE, Ewert M, Fransson A, Gosselin M (2015) Methods for biogeochemical studies of sea ice: the state of the art, caveats, and recommendations. Elem Sci Anth 3:1–53. doi:10.12952/journal.elementa.000038

    Article  Google Scholar 

  • Minikin A, Wagenbach D, Ducroz F, Mulvaney R, Keck L, Legrand M, Hall JS, Wolff EW (1998) Sea-salt aerosol in coastal Antarctic regions at three coastal. J Geophys Res 103:10961–10974

    Article  Google Scholar 

  • Mykytczuk NC, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG (2013) Bacterial growth at −15 °C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7:1211–1226. doi:10.1038/ismej.2013.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadeau T, Castenholz RW (2000) Characterization of psychrophilic Oscillatorians (cyanobacteria) from Antarctic meltwater ponds. J Phycol 923:914–923

    Article  Google Scholar 

  • Nadeau T-L, Milbrandt EC, Castenholz RW (2001) Evolutionary relationships of cultivated Antarctic Oscllatorians (Cyanobacteria). J Phycol 37:650–654

    Article  Google Scholar 

  • Nawrocki EP, Eddy SR (2013) Computational identification of functional RNA homologs in metagenomic data. RNA Biol 10:1170–1179. doi:10.4161/rna.25038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J, Finn RD (2015) Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 43:D130–D137. doi:10.1093/nar/gku1063

    Article  PubMed  Google Scholar 

  • Nkem JN, Wall DH, Virginia RA, Barrett JE, Broos EJ, Porazinska DL, Adams BJ (2006) Wind dispersal of soil invertebrates in the McMurdo Dry Valleys, Antarctica. Polar Biol 29:346–352. doi:10.1007/s00300-005-0061-x

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) vegan: Community Ecology Package. R package version 2.3-4. https://CRAN.R-project.org/package=vegan

  • Parker BC, Simmons GM, Wharton RA Jr, Seaburg KG, Love FG (1982) Removal of organic and inorganic matter from Antarctic lakes by aerial escape of bluegreen algal mats. J Phycol 18:72–78

    Article  Google Scholar 

  • Pasteris DR, McConnell JR, Das SB, Criscitiello AS, Evans MJ, Maselli OJ, Sigl M, Layman L (2014) Seasonally resolved ice core records from West Antarctica indicate a sea ice source of sea salt aerosol and a biomass burning source of ammonium. J Geophys Res Atmos 119:9168–9182. doi:10.1002/2013JD020720

    Article  CAS  Google Scholar 

  • Pearce DA, Hughes KA, Lachlan-Cope T, Harangozo SA, Jones AE (2010) Biodiversity of air-borne microorganisms at Halley station, Antarctica. Extremophiles 14:145–159. doi:10.1007/s00792-009-0293-8

    Article  PubMed  Google Scholar 

  • Porazinska DL, Fountain AG, Nylen TH, Tranter M, Virginia RA, Wall DH (2004) The biodiversity and biogeochemistry of cryoconite holes from McMurdo Dry Valley glaciers, Antarctica. Arct Antarct Alp Res 36:84–91

    Article  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi:10.1093/nar/gkm864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rankin AM (2002) Frost flowers: implications for tropospheric chemistry and ice core interpretation. J Geophys Res. doi:10.1029/2002JD002492

    Google Scholar 

  • Rankin AM, Auld V, Wolff EW (2000) Frost flowers as a source of fractionated sea salt aerosol in the polar regions. Geophys Res Lett 27:3469–3472

    Article  CAS  Google Scholar 

  • Šabacká M, Priscu JC, Basagic HJ, Fountain AG, Wall DH, Virginia RA, Greenwood MC (2012) Aeolian flux of biotic and abiotic material in Taylor Valley, Antarctica. Geomorphology 155–156:102–111. doi:10.1016/j.geomorph.2011.12.009

    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 Microb 75:7537–7541. doi:10.1128/AEM.01541-09

    Article  CAS  Google Scholar 

  • Shi Y, Tyson GW, Eppley JM, Delong EF (2010) Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean. ISME J 5:999–1013. doi:10.1038/ismej.2010.189

    Article  PubMed  PubMed Central  Google Scholar 

  • Sievert SM, Heidorn T, Kuever J (2000) Halothiobacillus kellyi sp. nov., a mesophilic, obligately chemolithoautotrophic, sulfur-oxidizing bacterium isolated from a shallow- water hydrothermal vent in the Aegean Sea, and emended description of the genus Halothiobacillus. Int J Syst Evol Microbiol 50:1229–1237. doi:10.1099/00207713-50-3-1229

    Article  CAS  PubMed  Google Scholar 

  • Soo RM, Wood SA, Grzymski JJ, McDonald IR, Cary SC (2009) Microbial biodiversity of thermophilic communities in hot mineral soils of Tramway Ridge, Mount Erebus, Antarctica. Environ Microbiol 11:715–728. doi:10.1111/j.1462-2920.2009.01859.x

    Article  CAS  PubMed  Google Scholar 

  • Sorokin DY, Kovaleva OL, Tourova TP, Muyzer G (2010) Thiohalobacter thiocyanaticus gen. nov., sp. nov., a moderately halophilic, sulfur-oxidizing gammaproteobacterium from hypersaline lakes, that utilizes thiocyanate. Int J Syst Evol Microbiol 60:444–450. doi:10.1099/ijs.0.012880-0

    Article  CAS  PubMed  Google Scholar 

  • Tang EPY, Tremblay R, Vincent WF (1997) Cyanobacterial dominance of polar freshwater ecosystems: are high-latitude mat-formers adapted to low temperature? J Phycol 181:171–181

    Article  Google Scholar 

  • Team RC (2014) R: A language and environment for statistical computing. http://www.r-project.org/. Accessed 1 Dec 2012

  • Tebo BM, Davis RE, Anitori RP, Connell LB, Schiffman P, Staudigel H (2015) Microbial communities in dark oligotrophic volcanic ice cave ecosystems of Mt. Erebus, Antarctica. Front Microbiol 6:1–14. doi:10.3389/fmicb.2015.00179

    Article  Google Scholar 

  • Wells LE, Deming JW (2006) Characterization of a cold-active bacteriophage on two psychrophilic marine hosts. Aquat Microb Ecol 45:15–29. doi:10.3354/ame045015

    Article  Google Scholar 

  • Whitaker D, Christman M (2014) clustsig: significant cluster analysis. http://cran.r-project.org/package=clustsig. Accessed 1 Mar 2016

  • Wolff EW (2003) An ice core indicator of Antarctic sea ice production? Geophys Res Lett 30:2–5. doi:10.1029/2003GL018454

    Article  Google Scholar 

  • Wright JJ, Konwar KM, Hallam SJ (2012) Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 10:381–394. doi:10.1038/nrmicro2778

    CAS  PubMed  Google Scholar 

  • Zmasek C (2014) Archaeopteryx. https://sites.google.com/site/cmzmasek/home/software/archaeopteryx. Accessed 1 Mar 2016

Download references

Acknowledgments

This work was supported by NSF PLR award 1043265 to J.W.D. and the Walters Endowed Professorship. J.S.B. was supported by an NSF IGERT Fellowship through the University of Washington’s Astrobiology Program and an EPA STAR Fellowship. We are grateful to Shelly Carpenter for her stalwart assistance with sample collections and processing in the field.

Author information

Authors and Affiliations

  1. School of Oceanography, University of Washington, Seattle, WA, USA

    Jeff S. Bowman & Jody W. Deming

  2. Lamont-Doherty Earth Observatory at Columbia University, Palisades, NY, USA

    Jeff S. Bowman

  3. Blue Marble Space Institute of Science, Seattle, WA, USA

    Jeff S. Bowman

Authors
  1. Jeff S. Bowman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jody W. Deming
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeff S. Bowman.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bowman, J.S., Deming, J.W. Wind-driven distribution of bacteria in coastal Antarctica: evidence from the Ross Sea region. Polar Biol 40, 25–35 (2017). https://doi.org/10.1007/s00300-016-1921-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-016-1921-2

Keywords

Search

Navigation