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Cyanobacterial Diversity and Halotolerance in a Variable Hypersaline Environment

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Abstract

The Great Salt Plains (GSP) in north-central Oklahoma, USA is an expansive salt flat (∼65 km2) that is part of the federally protected Salt Plains National Wildlife Refuge. The GSP serves as an ideal environment to study the microbial diversity of a terrestrial, hypersaline system that experiences wide fluctuations in freshwater influx and diel temperature. Our study assessed cyanobacterial diversity at the GSP by focusing on the taxonomic and physiological diversity of GSP isolates, and the 16S rRNA phylogenetic diversity of isolates and environmental clones from three sites (north, central, and south). Taxonomic diversity of isolates was limited to a few genera (mostly Phormidium and Geitlerinema), but physiological diversity based on halotolerance ranges was strikingly more diverse, even between strains of the same phylotype. The phylogenetic tree revealed diversity that spanned a number of cyanobacterial lineages, although diversity at each site was dominated by only a few phylotypes. Unlike other hypersaline systems, a number of environmental clones from the GSP were members of the heterocystous lineage. Although a number of cyanobacterial isolates were close matches with prevalent environmental clones, it is not certain if these clones reflect the same halotolerance ranges of their matching isolates. This caveat is based on the notable disparities we found between strains of the same phylotype and their inherent halotolerance. Our findings support the hypothesis that variable or poikilotrophic environments promote diversification, and in particular, select for variation in ecotype more than phylotype.

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References

  1. Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic Press, New York, New York, USA, p 608

    Google Scholar 

  2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Nucl Acids Res 25:3389–4402

    Article  PubMed  CAS  Google Scholar 

  3. Anagnostidis K, Komarek J (1988) Arch Hydrobiol Suppl 80:327–472

    Google Scholar 

  4. Ballot A, Dadheech PK, Krienitz L (2004) Arch Hydrobiol Suppl Algol Stud 113:37–56

    Google Scholar 

  5. Bauld J (1981) Hydrobiologia 81:87–111

    Article  Google Scholar 

  6. Beer S, Eshel A (1985) Aust J Mar Fresh Res 36:785–792

    Article  CAS  Google Scholar 

  7. Berman-Frank I, Lundgren P, Falkowski P (2003) Res Microbiol 154:157–164

    Article  PubMed  CAS  Google Scholar 

  8. Brock TD (1976) Arch Microbiol 107:109–111

    Article  PubMed  CAS  Google Scholar 

  9. Buchheim MA, Buchheim JA, Carlson T, Kugrens P (2002) J Phycol 38:376–383

    Article  CAS  Google Scholar 

  10. Buchheim MA, Chapman RL (1992) J Phycol 28:362–374

    Article  CAS  Google Scholar 

  11. Buchheim MA, Lemieux C, Otis C, Gutell RR, Chapman RL, Turmel M (1996) Mol Phylogenet Evol 5:391–402

    Article  PubMed  CAS  Google Scholar 

  12. Burke CM (1995) Microb Ecol 29:163–171

    Article  CAS  Google Scholar 

  13. Burns BP, Goh F, Allen M, Neilan BA (2004) Environ Microbiol 6:1096–1101

    Article  PubMed  CAS  Google Scholar 

  14. Campbell SE, Golubic S (1985) Arch Hydrobiol Suppl 71(38/39):311–329

    Google Scholar 

  15. Casillas-Martinez L, Gonzalez M, Fuentes-Figueroa Z, Castro C, Nieves-Mendez D, Hernandez C, Ramirez W, Sytsma R, Perez-Jimenez J, Visscher P (2005) Geomicrobiol J 22:269–281

    Article  CAS  Google Scholar 

  16. Caumette P (1993) Experientia 49:473–481

    Article  CAS  Google Scholar 

  17. Davis JS (1978) Aquat Bot 4:23–42

    Article  Google Scholar 

  18. Demergasso C, Chong G, Galleguillos P, Escudero L, Martinez-Alonso M, Esteve I (2003) Rev Chil Hist Nat 76:485–499

    Article  Google Scholar 

  19. Dubinin AV, Gerasimenko LM, Zavarzin GA (1992) Microbiology 61:593–597

    Google Scholar 

  20. Garcia-Pichel F, Nübel U, Muyzer G (1998) Arch Microbiol 169:469–482

    Article  PubMed  CAS  Google Scholar 

  21. Giraud A, Matic I, Tenaillon O, Clara A, Radman M, Fons M, Taddei F (2001) Science 291:2606–2608

    Article  PubMed  CAS  Google Scholar 

  22. Gorbushina AA, Krumbein WE (1999) Poikilotrophic response of microorganisms to shifting alkalinity, salinity, temperature and water potential. In: Oren A (ed) Microbiology and Biogeochemistry of Hypersaline Environments. CRC Press, Boca Raton, Florida, USA, p 359

    Google Scholar 

  23. Henley WJ, Levavasseur G, Franklin LA, Osmond CB, Ramus J (1991) Planta 184:235–243

    Article  CAS  Google Scholar 

  24. Henley WJ, Major KM, Hironaka JL (2002) J Phycol 38:757–766

    Article  Google Scholar 

  25. Jeffrey SW, Humphrey GF (1975) Biochem Physiol 167:191–194

    CAS  Google Scholar 

  26. Johnson KS (1980) Guidebook for Geologic Field Trips in Oklahoma. Book II: Northwest Oklahoma. University of Oklahoma, Norman, Oklahoma, USA

  27. Kirkwood AE, Henley WJ (2006) J Phycol 42:537–547

    Article  CAS  Google Scholar 

  28. Komarek J, Anagnostidis K (1986) Arch Hydrobiol Suppl 73:157–226

    Google Scholar 

  29. Maddison WP, Maddison DR (2001) MacClade. Sinauer Associates, Sunderland, MA, USA

    Google Scholar 

  30. McKenzie GJ, Rosenberg SM (2001) Curr Opin Microbiol 4:586–594

    Article  PubMed  CAS  Google Scholar 

  31. Moxon ER, Rainey PB, Nowak MA, Lenski RE (1994) Curr Biol 4:24–33

    Article  PubMed  CAS  Google Scholar 

  32. Nübel U, Garcia-Pichel F, Kühl M, Muyzer G (1999) Hydrobiol 401:199–206

    Article  Google Scholar 

  33. Nübel U, Garcia-Pichel F, Muyzer G (1997) Appl Environ Microbiol 63:3327–3332

    PubMed  Google Scholar 

  34. Nübel U, Garcia-Pichel F, Muyzer G (2000) Int J Syst Evol Microbiol 50:1265–1277

    PubMed  Google Scholar 

  35. Omoregie EO, Crumbliss LL, Bebout BM, Zehr JP (2004) FEMS Microbiol Ecol 47:305–318

    Article  CAS  Google Scholar 

  36. Oren A (2000) Salts and brines In: Whitton BA, Potts MA (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, The Netherlands. p. 281–306

    Google Scholar 

  37. Posada D, Crandall K (1998) Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  38. Potter AT, Palmer MW, Henley WJ (2006) Am Midl Nat 156:65–74

    Article  Google Scholar 

  39. Robertson BR, Tezuka N, Watanabe MM (2001) Int J Syst Evol Microbiol 51:861–867

    PubMed  CAS  Google Scholar 

  40. Rothschild LJ, Giver LJ, White MR, Mancinelli RL (1994) J Phycol 30:431–438

    Article  PubMed  CAS  Google Scholar 

  41. Sørensen KB, Canfield DE, Teske AP, Oren A (2005) Appl Environ Microbiol 71:7352–7365

    Article  PubMed  CAS  Google Scholar 

  42. Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Bacter Rev 35:171–205

    CAS  Google Scholar 

  43. Starr RC, Zeikus JA (1993) J Phycol 29(2 suppl.):90–91

    Google Scholar 

  44. Stolz JF (1990) Distribution of phototrophic microbes in the flat, laminated microbial mat at Laguna Figueroa, Baja California, Mexico. BioSystems 23:345–357

    Article  PubMed  CAS  Google Scholar 

  45. Swofford D (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*And Other Methods). Version 4. Sinauer Associates, Sunderland, MA, USA

    Google Scholar 

  46. Wilson C, TM Caton, JA Buchheim, MA Buchheim, MA Schneegurt, Miller RV (2004) Microb Ecol 48:541–549

    Article  PubMed  CAS  Google Scholar 

  47. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Biogeochem 57:1–45

    Article  Google Scholar 

  48. Wynn-Williams DD (2000) Cyanobacteria in deserts—Life at the limits? In: Whitton BA, Potts MA (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, The Netherlands p. 341–366

    Google Scholar 

  49. Yuan W (1989) Okla Geol Notes 49:200–223

    Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation’s Microbial Observatories program under grant nos. MCB-0132097 (WJH) and MCB-0132083 (MAB). We thank Andy Potter for assistance in the field and preparing the satellite image of the GSP. Karen Winans of the University of Tulsa Comparative Genomics Center performed automated sequencing. Finally, we wish to acknowledge our SPMO partners Robert Miller (Oklahoma State University) and Mark Schneegurt (Wichita State University) for their input and support.

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Authors and Affiliations

  1. Botany Department, Oklahoma State University, 104 Life Sciences East, Stillwater, OK, 74078, USA

    Andrea E. Kirkwood & William J. Henley

  2. Department of Biological Science and the Mervin Bovaird Institute for Molecular Biology and Biotechnology, The University of Tulsa, 600 South College Avenue, Tulsa, OK, 74104, USA

    Julie A. Buchheim & Mark A. Buchheim

  3. Department of Biological Sciences, University of Calgary, 2500 University Dr., Rm. 376B, NW Calgary, AB, T2N 1N4, Canada

    Andrea E. Kirkwood

  4. Department of Anatomy and Cell Biology, Center for Health Sciences, Oklahoma State University, Tulsa, OK, 74107, USA

    Julie A. Buchheim

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  1. Andrea E. Kirkwood
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  2. Julie A. Buchheim
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  3. Mark A. Buchheim
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  4. William J. Henley
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Correspondence to Andrea E. Kirkwood.

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Kirkwood, A.E., Buchheim, J.A., Buchheim, M.A. et al. Cyanobacterial Diversity and Halotolerance in a Variable Hypersaline Environment. Microb Ecol 55, 453–465 (2008). https://doi.org/10.1007/s00248-007-9291-5

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  • DOI: https://doi.org/10.1007/s00248-007-9291-5

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