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Bacterial diversity in permanently cold and alkaline ikaite columns from Greenland

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Abstract

Bacterial diversity in alkaline (pH 10.4) and permanently cold (4°C) ikaite tufa columns from the Ikka Fjord, SW Greenland, was investigated using growth characterization of cultured bacterial isolates with Terminal-restriction fragment length polymorphism (T-RFLP) and sequence analysis of bacterial 16S rRNA gene fragments. More than 200 bacterial isolates were characterized with respect to pH and temperature tolerance, and it was shown that the majority were cold-active alkaliphiles. T-RFLP analysis revealed distinct bacterial communities in different fractions of three ikaite columns, and, along with sequence analysis, it showed the presence of rich and diverse bacterial communities. Rarefaction analysis showed that the 109 sequenced clones in the 16S rRNA gene library represented between 25 and 65% of the predicted species richness in the three ikaite columns investigated. Phylogenetic analysis of the 16S rRNA gene sequences revealed many sequences with similarity to alkaliphilic or psychrophilic bacteria, and showed that 33% of the cloned sequences and 33% of the cultured bacteria showed less than 97% sequence identity to known sequences in databases, and may therefore represent yet unknown species.

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References

  • Bano N, Ruffin S, Ransom B, Hollibaugh JT (2004) Phylogenetic composition of Arctic ocean archaeal assemblages and comparison with Antarctic assemblages. Appl Environ Microbiol 70:781–789

    Article  PubMed  CAS  Google Scholar 

  • Bills GF, Polishook JD (1994) Abundance and diversity of microfungi in leaf-litter of a lowland rain-forest in Costa Rica. Mycologia 86:187–198

    Google Scholar 

  • Boetius A (2005) Lost City life. Science 307:1420–1422

    Article  PubMed  CAS  Google Scholar 

  • Brettar I, Christen R, Hofle MG (2004) Belliella baltica gen. nov., sp. nov., a novel marine bacterium of the Cytophaga-Flavobacterium-Bacteroides group isolated from surface water of the central Baltic Sea. Int J Syst Evol Microbiol 54:65–70

    Article  PubMed  CAS  Google Scholar 

  • Buchardt B, Seaman P, Stockmann G, Vous M, Wilken U, Düwel L, Kristiansen Aa, Jenner C, Whitticar MJ, Kristensen RM, Petersen GH, Thorbjørn L (1997) Submarine columns of ikaite tufa. Nature 390:129–130

    Article  CAS  Google Scholar 

  • Buchardt B, Israelson C, Seaman P, Stockmann G (2001) Ikaite tufa towers in Ikka Fjord, southwest Greenland: their formation by mixing of seawater and alkaline spring water. J Sediment Res 71:176–189

    CAS  Google Scholar 

  • Burnham KP, Overton WS (1979) Robust estimation of population size when capture probabilities vary among animals. Ecology 60:927–936

    Article  Google Scholar 

  • Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  • Chao A, Ma MC, Yang MCK (1993) Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika 80:193–201

    Article  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  PubMed  CAS  Google Scholar 

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E, Plymouth Marine Laboratory, Plymouth, UK

    Google Scholar 

  • Coleman BD, Mares MA, Willig MR, Hsieh Y-H (1982) Randomness, area, and species richness. Ecology 63:1121–1133

    Article  Google Scholar 

  • Colwell RK (2005) EstimateS: statistical estimation of species richness and shared species from samples. Version 7.5. User’s guide and application published at: http://www.purl.oclc.org/estimates

  • Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci USA 99:10494–10499

    Article  PubMed  CAS  Google Scholar 

  • Doronina NV, Darmaeva TD, Trotsenko TA (2003) Methylophaga alcalica sp. nov., a novel alkaliphilic and moderately halophilic, obligately methylotrophic bacterium from an East Mongolian saline soda lake. Int J Syst Evol Microbiol 53:223–229

    Article  PubMed  CAS  Google Scholar 

  • Duckworth AW, Grant WD, Jones BE, van Steenbergen R (1996) Phylogenetic diversity of soda lake alkaliphiles. FEMS Microbiol Ecol 19:181–191

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hoover RB, Pikuta EV, Bej AK, Marsic D, Whitman WB, Tang J, Krader P (2003) Spirochaeta americana sp. nov., a new haloalkaliphilic, obligately anaerobic spirochaete isolated from soda Mono Lake in California. Int J Syst Evol Microbiol 53:815–821

    Article  PubMed  CAS  Google Scholar 

  • Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67:4399–4406

    Article  PubMed  CAS  Google Scholar 

  • Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586

    Article  Google Scholar 

  • Jones BE, Grant WD, Duckworth AW, Owenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2:191–200

    Article  PubMed  CAS  Google Scholar 

  • Kelley DS, Karson JA, Blackman DK, Früh-Green GL, Butterfield DA, Lilley MD, Olson EJ, Schrenk MO, Roe KK, Lebon GT, Rivizzigno P (2001) An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30°N. Nature 412:145–149

    Article  PubMed  CAS  Google Scholar 

  • Kristiansen J, Kristiansen Aa (1999) A new species of Chroomonas (Cryptophyceae) living inside the submarine ikaite columns in the Ikka fjord, Southwest Greenland, with remarks on its ultrastructure and ecology. Nordic J Bot 19:747–758

    Article  Google Scholar 

  • Kroes I, Lepp PW, Relman DA (1999) Bacterial diversity within the human subgingival crevice. Proc Natl Acad Sci USA 96:14547–14552

    Article  PubMed  CAS  Google Scholar 

  • Ma Y, Xue Y, Grant WD, Collins NC, Duckworth AW, van Steenbergen RP, Jones BE (2004) Alkalimonas amylolytica gen. nov., sp. nov., and Alkalimonas delamerensis gen. nov., sp. nov., novel alkaliphilic bacteria from soda lakes in China and East Africa. Extremophiles 8:193–200

    Article  PubMed  CAS  Google Scholar 

  • Maidak BL, Olsen GJ, Larsen N, Overbeek R, McCaughey MJ, Woese CR (1997) The RDP (ribosomal database project). Nucleic Acids Res 25:109–110

    Article  PubMed  CAS  Google Scholar 

  • Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218

    Article  CAS  Google Scholar 

  • Milford AD, Achenbach LA, Jung DO, Madigan MT (2000) Rhodobaca bogoriensis gen. nov. and sp. nov., an alkaliphilic purple nonsulfur bacterium from African rift valley soda lakes. Arch Microbiol 174:18–27

    Article  PubMed  CAS  Google Scholar 

  • Moyer CL, Tiedje JM, Dobbs FC, Karl DM (1998) Diversity of deep-sea hydrothermal vent Archaea from Loihi seamount, Hawaii. Deep-Sea Res II 45:303–317

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nielsen P, Fritze D, Priest EG (1995) Phenetic diversity of alkaliphilic Bacillus strains: proposal for nine new species. Microbiology 141:1745–1761

    Article  CAS  Google Scholar 

  • Pauly H (1963) Ikaite, a new mineral from Greenland. Arctic 16:263–264

    CAS  Google Scholar 

  • Priemé A, Braker G, Tiedje JM (2002) Diversity of nitrite reductase (nirK and nirS) gene fragments in forested upland and wetland soils. Appl Environ Microbiol 68:1893–1900

    Article  PubMed  CAS  Google Scholar 

  • Rees HC, Grant WD, Jones BE, Heaphy S (2004) Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8:63–71

    Article  PubMed  CAS  Google Scholar 

  • Schrenk MO, Kelley DS, Bolton SA, Baross JA (2004) Low archaeal diversity linked to subseafloor geochemical processes at the Lost City hydrothermal field, Mid-Atlantic ridge. Environ Microbiol 6:1086–1095

    Article  PubMed  CAS  Google Scholar 

  • Smith EP, vanBelle G (1984) Non-parametric estimation of species richness. Biometrics 40:119–129

    Article  Google Scholar 

  • Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen GJ (2001) Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp.nov., and Thioalkalivibrio denitrificancs sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 51:565–580

    PubMed  CAS  Google Scholar 

  • Sorokin DY, Tourova TP, Lysenko AM, Mityushina LL, Kuenen JG (2002) Thioalkalivibrio thiocyanoxidans sp. nov. and Thioalkalivibrio paradoxus sp. nov., novel alkaliphilic, obligately autotrophic, sulphur-oxidizing bacteria capable of growth on thiocyanate, from soda lakes. Int J Syst Evol Microbiol 52:657–664

    PubMed  CAS  Google Scholar 

  • Sorokin DY, Banciu H, van Loosdrecht M, Kuenen JG (2003) Growth physiology and competitive interaction of obligately chemolithoautotrophic, haloalkaliphilic, sulphur-oxidizing bacteria from soda lakes. Extremophiles 7:195–203

    PubMed  Google Scholar 

  • Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    Article  CAS  Google Scholar 

  • Stockmann G, Buchardt B, Kristiansen Aa (2000) The submarine ikaite column garden in Ikka Fjord, SW Greenland. Northern Science Network Newsletter no. 26/27. Danish Polar Center, Copenhagen

    Google Scholar 

  • Stougaard P, Jørgensen F, Johnsen MG, Hansen OC (2002) Microbial diversity in ikaite tufa columns: an alkaline, cold ecological niche in Greenland. Environ Microbiol 4:487–493

    Article  PubMed  CAS  Google Scholar 

  • Sørensen MV, Kristensen RM (2000) Marine rotifera from Ikka Fjord, SW Greenland. With a description of a new species from the rare mineral ikaite. Monographs on Greenland/Meddelelser om Grønland. Bioscience 51

  • Thorbjørn L, Petersen GH (2003) The epifauna on the carbonate reefs in the Arctic Ikka Fjord, SW Greenland. Ophelia 57:177–202

    Google Scholar 

  • Tiago I, Chung AP, Veríssimo A (2004) Bacterial diversity in a nonsaline alkaline environment: heterotrophic aerobic populations. Appl Environ Microbiol 70:7378–7387

    Article  PubMed  CAS  Google Scholar 

  • Van de Peer Y, De Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570

    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  CAS  Google Scholar 

  • Yakimov MM, Giuliano L, Chernikova TN, Gentile G, Abraham W-R, Lünsdorf H, Timmis KN, Golyshin PN (2001) Alkalimonas halodurans gen. nov., sp. nov., an alkaliphilic, moderately halophilic and extremely halotolerant bacterium, isolated from sediments of soda-depositing Lake Natron, East Africa rift valley. Int J Syst Evol Microbiol 51:2133–2143

    PubMed  CAS  Google Scholar 

  • Zhilina TN, Appel R, Probian C, Brossa EL, Harder J, Widdel F, Zavarzin GA (2004) Alkaliflexus imshenetskii gen. nov. sp. nov., a new alkaliphilic gliding carbohydrate-fermenting bacterium with propionate formation from a soda lake. Arch Microbiol 182:244–253

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Brunns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Bente M. Smith and Karin Vestberg for excellent technical skills, Mads Johnsen and Flemming Jørgensen for stimulating discussions. Referring to the Convention on Biological Diversity, we thank the Greenland Home Rule for permission to sample ikaite columns from the Ikka Fjord, SW Greenland. This work was partly funded by the Danish Agency for Trade and Industry (MS and PS) and by the Oticon foundation (MS).

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Correspondence to Peter Stougaard.

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Communicated by A. Driessen

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Schmidt, M., Priemé, A. & Stougaard, P. Bacterial diversity in permanently cold and alkaline ikaite columns from Greenland. Extremophiles 10, 551–562 (2006). https://doi.org/10.1007/s00792-006-0529-9

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