Microbial Ecology

, Volume 55, Issue 3, pp 453–465 | Cite as

Cyanobacterial Diversity and Halotolerance in a Variable Hypersaline Environment

  • Andrea E. Kirkwood
  • Julie A. Buchheim
  • Mark A. Buchheim
  • William J. Henley
Original Article

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.

References

  1. 1.
    Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic Press, New York, New York, USA, p 608Google Scholar
  2. 2.
    Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Nucl Acids Res 25:3389–4402PubMedCrossRefGoogle Scholar
  3. 3.
    Anagnostidis K, Komarek J (1988) Arch Hydrobiol Suppl 80:327–472Google Scholar
  4. 4.
    Ballot A, Dadheech PK, Krienitz L (2004) Arch Hydrobiol Suppl Algol Stud 113:37–56Google Scholar
  5. 5.
    Bauld J (1981) Hydrobiologia 81:87–111CrossRefGoogle Scholar
  6. 6.
    Beer S, Eshel A (1985) Aust J Mar Fresh Res 36:785–792CrossRefGoogle Scholar
  7. 7.
    Berman-Frank I, Lundgren P, Falkowski P (2003) Res Microbiol 154:157–164PubMedCrossRefGoogle Scholar
  8. 8.
    Brock TD (1976) Arch Microbiol 107:109–111PubMedCrossRefGoogle Scholar
  9. 9.
    Buchheim MA, Buchheim JA, Carlson T, Kugrens P (2002) J Phycol 38:376–383CrossRefGoogle Scholar
  10. 10.
    Buchheim MA, Chapman RL (1992) J Phycol 28:362–374CrossRefGoogle Scholar
  11. 11.
    Buchheim MA, Lemieux C, Otis C, Gutell RR, Chapman RL, Turmel M (1996) Mol Phylogenet Evol 5:391–402PubMedCrossRefGoogle Scholar
  12. 12.
    Burke CM (1995) Microb Ecol 29:163–171CrossRefGoogle Scholar
  13. 13.
    Burns BP, Goh F, Allen M, Neilan BA (2004) Environ Microbiol 6:1096–1101PubMedCrossRefGoogle Scholar
  14. 14.
    Campbell SE, Golubic S (1985) Arch Hydrobiol Suppl 71(38/39):311–329Google Scholar
  15. 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 22:269–281CrossRefGoogle Scholar
  16. 16.
    Caumette P (1993) Experientia 49:473–481CrossRefGoogle Scholar
  17. 17.
    Davis JS (1978) Aquat Bot 4:23–42CrossRefGoogle Scholar
  18. 18.
    Demergasso C, Chong G, Galleguillos P, Escudero L, Martinez-Alonso M, Esteve I (2003) Rev Chil Hist Nat 76:485–499CrossRefGoogle Scholar
  19. 19.
    Dubinin AV, Gerasimenko LM, Zavarzin GA (1992) Microbiology 61:593–597Google Scholar
  20. 20.
    Garcia-Pichel F, Nübel U, Muyzer G (1998) Arch Microbiol 169:469–482PubMedCrossRefGoogle Scholar
  21. 21.
    Giraud A, Matic I, Tenaillon O, Clara A, Radman M, Fons M, Taddei F (2001) Science 291:2606–2608PubMedCrossRefGoogle Scholar
  22. 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 359Google Scholar
  23. 23.
    Henley WJ, Levavasseur G, Franklin LA, Osmond CB, Ramus J (1991) Planta 184:235–243CrossRefGoogle Scholar
  24. 24.
    Henley WJ, Major KM, Hironaka JL (2002) J Phycol 38:757–766CrossRefGoogle Scholar
  25. 25.
    Jeffrey SW, Humphrey GF (1975) Biochem Physiol 167:191–194Google Scholar
  26. 26.
    Johnson KS (1980) Guidebook for Geologic Field Trips in Oklahoma. Book II: Northwest Oklahoma. University of Oklahoma, Norman, Oklahoma, USAGoogle Scholar
  27. 27.
    Kirkwood AE, Henley WJ (2006) J Phycol 42:537–547CrossRefGoogle Scholar
  28. 28.
    Komarek J, Anagnostidis K (1986) Arch Hydrobiol Suppl 73:157–226Google Scholar
  29. 29.
    Maddison WP, Maddison DR (2001) MacClade. Sinauer Associates, Sunderland, MA, USAGoogle Scholar
  30. 30.
    McKenzie GJ, Rosenberg SM (2001) Curr Opin Microbiol 4:586–594PubMedCrossRefGoogle Scholar
  31. 31.
    Moxon ER, Rainey PB, Nowak MA, Lenski RE (1994) Curr Biol 4:24–33PubMedCrossRefGoogle Scholar
  32. 32.
    Nübel U, Garcia-Pichel F, Kühl M, Muyzer G (1999) Hydrobiol 401:199–206CrossRefGoogle Scholar
  33. 33.
    Nübel U, Garcia-Pichel F, Muyzer G (1997) Appl Environ Microbiol 63:3327–3332PubMedGoogle Scholar
  34. 34.
    Nübel U, Garcia-Pichel F, Muyzer G (2000) Int J Syst Evol Microbiol 50:1265–1277PubMedGoogle Scholar
  35. 35.
    Omoregie EO, Crumbliss LL, Bebout BM, Zehr JP (2004) FEMS Microbiol Ecol 47:305–318CrossRefGoogle Scholar
  36. 36.
    Oren A (2000) Salts and brines In: Whitton BA, Potts MA (eds) The ecology of cyanobacteria. Kluwer Academic Publishers, The Netherlands. p. 281–306Google Scholar
  37. 37.
    Posada D, Crandall K (1998) Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  38. 38.
    Potter AT, Palmer MW, Henley WJ (2006) Am Midl Nat 156:65–74CrossRefGoogle Scholar
  39. 39.
    Robertson BR, Tezuka N, Watanabe MM (2001) Int J Syst Evol Microbiol 51:861–867PubMedGoogle Scholar
  40. 40.
    Rothschild LJ, Giver LJ, White MR, Mancinelli RL (1994) J Phycol 30:431–438PubMedCrossRefGoogle Scholar
  41. 41.
    Sørensen KB, Canfield DE, Teske AP, Oren A (2005) Appl Environ Microbiol 71:7352–7365PubMedCrossRefGoogle Scholar
  42. 42.
    Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Bacter Rev 35:171–205Google Scholar
  43. 43.
    Starr RC, Zeikus JA (1993) J Phycol 29(2 suppl.):90–91Google Scholar
  44. 44.
    Stolz JF (1990) Distribution of phototrophic microbes in the flat, laminated microbial mat at Laguna Figueroa, Baja California, Mexico. BioSystems 23:345–357PubMedCrossRefGoogle Scholar
  45. 45.
    Swofford D (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*And Other Methods). Version 4. Sinauer Associates, Sunderland, MA, USAGoogle Scholar
  46. 46.
    Wilson C, TM Caton, JA Buchheim, MA Buchheim, MA Schneegurt, Miller RV (2004) Microb Ecol 48:541–549PubMedCrossRefGoogle Scholar
  47. 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 57:1–45CrossRefGoogle Scholar
  48. 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. 341–366Google Scholar
  49. 49.
    Yuan W (1989) Okla Geol Notes 49:200–223Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Andrea E. Kirkwood
    • 1
    • 3
  • Julie A. Buchheim
    • 2
    • 4
  • Mark A. Buchheim
    • 2
  • William J. Henley
    • 1
  1. 1.Botany DepartmentOklahoma State UniversityStillwaterUSA
  2. 2.Department of Biological Science and the Mervin Bovaird Institute for Molecular Biology and BiotechnologyThe University of TulsaTulsaUSA
  3. 3.Department of Biological SciencesUniversity of CalgaryNW CalgaryCanada
  4. 4.Department of Anatomy and Cell Biology, Center for Health SciencesOklahoma State UniversityTulsaUSA

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