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Temporal, regional and geochemical drivers of microbial community variation in the melt ponds of the Ross Sea region, Antarctica

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Abstract

To expand the understanding of the poorly described planktonic bacterial communities inhabiting Antarctic meltwater ponds, this study characterized the community composition and identified environmental drivers influencing community structure from a total of 41 meltwater ponds: 37 from the McMurdo Ice Shelf (Bratina Island) and four from a terrestrial locale (Miers Valley) during three austral summers. DNA fingerprinting coupled with in situ pH and conductivity was utilized to select ponds for in-depth nutrient and chemical analysis and high-throughput sequencing of the bacterial 16S rRNA gene V5–V6 hypervariable region. Conductivity was the strongest driver of community structure across all ponds and for all time points; however, other influential factors (pH, climatological, Hg, Fe, and PO4) were also identified. Unique members of communities (sequences absent in at least one pond) represented a small percentage of total reads but also represented a large proportion of pond biodiversity that was strongly driven by differing environmental variables (Si, B and S). Significant temporal variation in community structure was also identified within the same ponds although major taxa remained present. Miers Valley ponds exhibit greater similarity to Bratina Island ponds rather than between each other, thereby suggesting regional movement of microorganisms. In summary, these data provide the first in-depth investigation of the intra-seasonal and regional variation of the microbial communities inhabiting these ponds and proved that a total of ten cosmopolitan OTUs were the dominant components of ponds throughout all sampling times and locations, their variable relative abundances driving the major dissimilarities in community structure.

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References

  • Abdo Z, Schuette UME, Bent SJ, Williams CJ, Forney LJ, Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938

    Article  PubMed  Google Scholar 

  • Archer S, McDonald I, Herbold C, Cary S (2014) Characterization of bacterioplankton communities in the melt-water ponds of Bratina Island, Victoria Land, Antarctica. FEMS Microbiol Ecol 89:451–464

    Article  CAS  PubMed  Google Scholar 

  • Ashby MN, Rine J, Mongodin EF, Nelson KE, Dimster-Denk D (2007) Serial analysis of rRNA genes and the unexpected dominance of rare members of microbial communities. Appl Environ Microbiol 73:4532–4542

    Article  PubMed Central  CAS  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

    Article  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

    Article  PubMed Central  PubMed  Google Scholar 

  • Cannone N, Wagner D, Hubberten HW, Guglielmin M (2008) Biotic and abiotic factors influencing soil properties across a latitudinal gradient in Victoria Land, Antarctica. Geoderma 144:50–65

    Article  CAS  Google Scholar 

  • Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, Zanardini E, Sorlini C, Corselli C, Daffonchio D (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70:6147–6156

    Article  PubMed Central  CAS  PubMed  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 

  • Chong CW, Goh YS, Convey P, Pearce D, Tan IKP (2013) Spatial pattern in Antarctica: what can we learn from Antarctic bacterial isolates? Extremophiles 17:733–745

    Article  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2006) Primer V6: User Manual/Tutorial PRIMER-E

  • Cowan DA, Tow LA (2004) Endangered Antarctic environments. Annu Rev Microbiol 58:649–690

    Article  CAS  PubMed  Google Scholar 

  • Coyne KJ, Hutchins DA, Hare CE, Cary SC (2001) Assessing temporal and spatial variability in Pfiesteria piscicida distributions using molecular probing techniques. Aquat Microb Ecol 24:275–285

    Article  Google Scholar 

  • De Bie T, De Meester L, Brendonck L, Martens K, Goddeeris B, Ercken D, Hampel H, Denys L, Vanhecke L, Van der Gucht K, Van Wichelen J, Vyverman W, Declerck SAJ (2012) Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol Lett 15:740–747

    Article  PubMed  Google Scholar 

  • De Mora SJ, Whitehead RF, Gregory M (1994) The chemical-composition of glacial melt water ponds and streams on the McMurdo Ice Shelf, Antarctica. Antarct Sci 6:17–27

    Article  Google Scholar 

  • Dempster EL, Pryor KV, Francis D, Young JE, Rogers HJ (1999) Rapid DNA extraction from ferns for PCR-based analyses. Biotechniques 27:66–68

    CAS  PubMed  Google Scholar 

  • Desai D, Desai F, LaRoche J (2012) Factors influencing the diversity of iron uptake systems in aquatic microorganisms. Front Microbiol. doi:10.3389/fmicb.2012.00362

    PubMed Central  PubMed  Google Scholar 

  • Dore JE, Priscu JC (2001) Phytoplankton phosphorus deficiency and alkaline phosphatase activity in the McMurdo Dry Valley lakes, Antarctica. Limnol Oceanogr 46:1331–1346

    Article  CAS  Google Scholar 

  • Dunbar GB, Bertler NAN, McKay RM (2009) Sediment flux through the McMurdo Ice Shelf in Windless Bight, Antarctica. Glob Planet Change 69:87–93

    Article  Google Scholar 

  • Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fitzsimons S, Mager S, Frew R, Clifford A, Wilson G (2012) Formation of ice-shelf moraines by accretion of sea water and marine sediment at the southern margin of the McMurdo Ice Shelf, Antarctica. Ann Glaciol 53:211–220

    Article  CAS  Google Scholar 

  • Foreman CM, Dieser M, Greenwood M, Cory RM, Laybourn-Parry J, Lisle JT, Jaros C, Miller PL, Chin YP, McKnight DM (2010) When a habitat freezes solid: microorganisms over-winter within the ice column of a coastal Antarctic lake. FEMS Microbiol Ecol 76:401–412

    Article  Google Scholar 

  • Gibson JAE, Wilmotte A, Taton A, Van der Vijver B, Beyens L, Dartnall HJG (2006) Biogeographic trends in Antarctic lake communities. In: Bergstrom DM, Convey P, Huskies HL (eds) Trends in Antarctic terrestrial and limnectic ecosystems: Antarctica as a global indicator. Springer, The Netherlands, pp 71–99

    Chapter  Google Scholar 

  • Hawes I, Smith R, Howard-Williams C, Schwarz AM (1999) Environmental conditions during freezing, and response of microbial mats in ponds of the McMurdo Ice Shelf, Antarctica. Antarct Sci 11:198–208

    Article  Google Scholar 

  • Hawes I, Safi K, Webster-Brown J, Sorrell B, Arscott D (2011a) Summer–winter transitions in Antarctic ponds II: biological responses. Antarct Sci 23:243–254

    Article  Google Scholar 

  • Hawes I, Safi K, Sorrell B, Webster-Brown J, Arscott D (2011b) Summer–winter transitions in Antarctic ponds I: the physical environment. Antarct Sci 23:235–242

    Article  Google Scholar 

  • Hawes I, Howard-Williams C, Sorrell B (2014) Decadal timescale variability in ecosystem properties in the ponds of the McMurdo Ice Shelf, southern Victoria Land, Antarctica. Antarct Sci 26:219–230

    Article  Google Scholar 

  • Healy M, Webster-Brown JG, Brown KL, Lane V (2006) Chemistry and stratification of Antarctic meltwater ponds II: Inland ponds in the McMurdo Dry Valleys, Victoria Land. Antarct Sci 18:525–533

    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. doi:10.1038/ncomms4875

    PubMed  Google Scholar 

  • Howard-Williams C, Pridmore R, Downes MT, Vincent WF (1989) Microbial biomass, photosynthesis and chlorophyll—A related pigments in the ponds of the McMurdo Ice Shelf, Antarctica. Antarct Sci 1:125–131

    Article  Google Scholar 

  • Howard-Williams C, Pridmore R, Broady P, Vincent WF (1990) Environmental and biological variability in the McMurdo Ice Shelf ecosystem. In: Kerry K, Hempel G (eds) Antarctic ecosystems. Springer, Berlin, pp 23–31

    Chapter  Google Scholar 

  • James MR, Pridmore RD, Cummings VJ (1995) Planktonic communities of melt ponds on the McMurdo ice shelf, Antarctica. Polar Biol 15:555–567

    Article  Google Scholar 

  • Jungblut AD, 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

    Article  CAS  PubMed  Google Scholar 

  • Jungblut AD, Lovejoy C, Vincent WF (2010) Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J 4:191–202

    Article  CAS  PubMed  Google Scholar 

  • Kellogg DE, Kellogg TB (1987) Diatoms of the McMurdo Ice Shelf, Antarctica: implications for sediment and biotic reworking. Palaeogeography 60:77–96

    Article  Google Scholar 

  • Kellogg TB, Kellogg DE (1988) Antarctic cryogenic sediments: biotic and inorganic facies of ice shelf and marine-based ice sheet environments. Palaeogeography 67:51–74

    Article  Google Scholar 

  • Kong W, Li W, Prášil O, Romancova I, Morgan-Kiss RM (2014) An integrated study of photochemical function and expression of a key photochemical gene (psbA) in photosynthetic communities of Lake Bonney (McMurdo Dry Valleys, Antarctica). FEMS Microbiol Ecol 89:293–302

    Article  CAS  PubMed  Google Scholar 

  • Lee CK, Barbier BA, Bottos EM, McDonald IR, Cary SC (2012) The inter-valley soil comparative survey: the ecology of dry valley edaphic microbial communities. ISME J 6:1046–1057

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu X, Wang B, Jiang C, Liu S (2008) Ornithinimicrobium pekingense sp nov., isolated from activated sludge. Int J Syst Evol Microbiol 58:116–119

    Article  CAS  PubMed  Google Scholar 

  • Lizotte MP, Priscu JC (1992) Photosynthesis irradiance relationships in Phytoplankton from the physically stable water column of a perennially ice-covered lake (Lake Bonney, Antarctica). J Phycol 28:179–185

    Article  Google Scholar 

  • Lyons WB, Welch KA, Gardner CB, Jaros C, Moorhead DL, Knoepfle JL, Doran PT (2012) The geochemistry of upland ponds, Taylor Valley, Antarctica. Antarct Sci 24:3–14

    Article  Google Scholar 

  • Ma B, Lv X, Warren A, Gong J (2013) Shifts in diversity and community structure of endophytic bacteria and archaea across root, stem and leaf tissues in the common reed, Phragmites australis, along a salinity gradient in a marine tidal wetland of northern China. Antonie Van Leeuwenhoek 104:759–768

    Article  PubMed  Google Scholar 

  • Matsumoto GI, Kakaya S, Murayama H, Masuda N, Kawano T, Watanuki K, Torii T (1992) Geochemical characteristics of Antarctic lakes and ponds. NIPR Polar Biol 5:125–145

    Google Scholar 

  • McLeod M, Bockheim J, Balks M, Aislabie J (2009) Soils of western Wright Valley, Antarctica. Antarct Sci 21:355–365

    Article  Google Scholar 

  • Moorhead DL, Wolf CF, Wharton RA (1997) Impact of light regimes on productivity patterns of benthic microbial mats in an Antarctic lake: a modeling study. Linol Oceanogr 42:1561–1569

    Article  CAS  Google Scholar 

  • Moorhead DL, Barrett JE, Virginia RA, Wall DH, Porazinska D (2003) Organic matter and soil biota of upland wetlands in Taylor Valley, Antarctica. Polar Biol 26:567–576

    Article  Google Scholar 

  • Nedashkovskaya OI, Vancanneyt M, Van Trappen S, Vandemeulebroecke K, Lysenko AM, Rohde M, Falsen E, Frolova GM, Mikhailov VV, Swings J et al (2004) Description of Algoriphagus aquimarinus sp nov., Algoriphagus chordae sp nov and Algoriphagus winogradskyi sp nov., from sea water and algae, transfer of Hongiella halophila Yi and Chun 2004 to the genus Algoriphagus as Algoriphagus halophilus comb. nov and emended descriptions of the genera Algoriphagus Bowman et al. 2003 and Hongiella Yi and Chun 2004. Int J Syst Evol Microbiol 54:1757–1764

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J (2011) Multivariate analysis of ecological communities in R: vegan tutorial. R package Version 2-0:

  • Pearce DA (2005) The structure and stability of the bacterioplankton community in Antarctic freshwater lakes, subject to extremely rapid environmental change. FEMS Microbiol Ecol 53:61–72

    Article  CAS  PubMed  Google Scholar 

  • Peeters K, Verleyen E, Hodgson DA, Convey P, Ertz D, Vyverman W, Willems A (2012) Heterotrophic bacterial diversity in aquatic microbial mat communities from Antarctica. Polar Biol 35:543–554

    Article  Google Scholar 

  • Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM, Read LF, Sloan WT (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6:639–641

    Article  CAS  PubMed  Google Scholar 

  • Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38

    Article  PubMed Central  PubMed  Google Scholar 

  • R_Core_Team (2013) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/

  • Sabacka M, Elster J (2006) Response of cyanobacteria and algae from Antarctic wetland habitats to freezing and desiccation stress. Polar Biol 30:31–37

    Article  Google Scholar 

  • Sabbe K, Hodgson DA, Verleyen E, Taton A, Wilmotte A, Vanhoutte K, Vyverman W (2004) Salinity, depth and the structure and composition of microbial mats in continental Antarctic lakes. Freshw Biol 49:296–319

    Article  Google Scholar 

  • Safi K, Hawes I, Sorrell B (2012) Microbial population responses in three stratified Antarctic meltwater ponds during the autumn freeze. Antarct Sci 24:571–588

    Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EM, 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Schmidt S, Moskal W, Demora SJ, Howard-Williams C, Vincent WF (1991) Limnological properties of Antarctic ponds during winter freezing. Antarct Sci 3:379–388

    Article  Google Scholar 

  • Schmidt SK, Nemergut DR, Miller AE, Freeman KR, King AJ, Seimon A (2009) Microbial activity and diversity during extreme freeze–thaw cycles in periglacial soils, 5400 m elevation, Cordillera Vilcanota, PerA(0). Extremophiles 13:807–816

    Article  CAS  PubMed  Google Scholar 

  • Silver S, Hobman J (2007) Molecular microbiology of heavy metals. In: Nies D, Silver S (eds) Mercury microbiology: resistance systems, environmental aspects, methylation, and human health, vol 6. Springer, Berlin, pp 357–370

    Google Scholar 

  • Sokol ER, Herbold CW, Lee CK, Cary SC, Barrett JE (2013) Local and regional influences over soil microbial metacommunities in the transantarctic mountains. Ecosphere, 4: art136

  • Sorrell BK, Hawes I, Safi K (2013) Nitrogen and carbon limitation of planktonic primary production and phytoplankton-bacterioplankton coupling in ponds on the McMurdo Ice Shelf, Antarctica. Enviro Res Lett 8:035043

    Article  Google Scholar 

  • Stanish LF, Kohler TJ, Esposito RMM, Simmons BL, Nielsen UN, Wall DH, Nemergut DR, McKnight DM (2012) Extreme streams: flow intermittency as a control on diatom communities in meltwater streams in the McMurdo Dry Valleys, Antarctica. Can J Fish Aquat Sci 69:1405–1419

    Article  Google Scholar 

  • Sun LJ, Cai YP, Liu L, Yu FH, Farrell ML, McKendree W, Farmerie W (2009) ESPRIT: estimating species richness using large collections of 16S rRNA pyrosequences. Nucleic Acids Res 37:e76

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Trappen S, Mergaert J, Swings J (2004) Loktanella salsilacus gen. nov., sp nov., Loktanella fryxellensis sp nov and Loktanella vestfoldensis sp nov., new members of the Rhodobacter group, isolated from microbial mats in Antarctic lakes. Int J Syst Evol Microbiol 54:1263–1269

    Article  PubMed  Google Scholar 

  • Vick-Majors TJ, Priscu JC, Amaral-Zettler LA (2014) Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes. ISME J 8:778–789

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vincent WF (2000) Evolutionary origins of Antarctic microbiota: invasion, selection and endemism. Antarct Sci 12:374–385

    Article  Google Scholar 

  • Vincent WF, James MR (1996) Biodiversity in extreme aquatic environments: lakes, ponds and streams of the Ross Sea Sector, Antarctica. Biodivers Conserv 5:1451–1471

    Article  Google Scholar 

  • Wait BR, Webster-Brown JG, Brown KL, Healy M, Hawes I (2006) Chemistry and stratification of Antarctic meltwater ponds I: coastal ponds near Bratina Island, McMurdo Ice Shelf. Antarct Sci 18:515–524

    Article  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Webster-Brown J, Hawes I, Safi K, Sorrell B, Wilson N (2012) Summer-winter transitions in Antarctic ponds: III. Chemical changes. Antarct Sci 24:121–130

    Article  Google Scholar 

  • Wood SA, Rueckert A, Cowan DA, Cary SC (2008) Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica. ISME J 2:308–320

    Article  CAS  PubMed  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 

  • Yi HN, Chun J (2006) Flavobacterium weaverense sp nov and Flavobacterium segetis sp nov., novel psychrophiles isolated from the Antarctic. Int J Syst Evol Microbiol 56:1239–1244

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Gao G, Tang X, Shao K, Bayartu S, Dai J (2013) Bacterial community changes along a salinity gradient in a Chinese wetland. Canadian J Microbiol 59:611–619

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by the International Centre for Terrestrial Antarctic Research, the University of Waikato, Antarctica New Zealand and New Zealand Post. Logistical support was provided by Antarctica New Zealand through their postgraduate research program.

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Authors and Affiliations

  1. International Centre for Terrestrial Antarctic Research, School of Science, University of Waikato, Private Bag 3105, Hamilton, New Zealand

    Stephen D. J. Archer, Ian R. McDonald, Craig W. Herbold, Charles K. Lee & Thomas S. Niederberger

  2. School of Science, University of Waikato, Private Bag 3105, Hamilton, 3240, New Zealand

    Craig Cary

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  1. Stephen D. J. Archer
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  2. Ian R. McDonald
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  3. Craig W. Herbold
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  4. Charles K. Lee
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  5. Thomas S. Niederberger
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  6. Craig Cary
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Correspondence to Stephen D. J. Archer.

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Archer, S.D.J., McDonald, I.R., Herbold, C.W. et al. Temporal, regional and geochemical drivers of microbial community variation in the melt ponds of the Ross Sea region, Antarctica. Polar Biol 39, 267–282 (2016). https://doi.org/10.1007/s00300-015-1780-2

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