Extremophiles

, Volume 9, Issue 4, pp 263–274 | Cite as

Bacterial diversity and carbonate precipitation in the giant microbialites from the highly alkaline Lake Van, Turkey

  • Purificación López-García
  • Józef Kazmierczak
  • Karim Benzerara
  • Stephan Kempe
  • François Guyot
  • David Moreira
Original Paper

Abstract

Lake Van harbors the largest known microbialites on Earth. The surface of these huge carbonate pinnacles is covered by coccoid cyanobacteria whereas their central axis is occupied by a channel through which neutral, relatively Ca-enriched, groundwater flows into highly alkaline (pH ~9.7) Ca-poor lake water. Previous microscopy observations showed the presence of aragonite globules composed by rounded nanostructures of uncertain origin that resemble similar bodies found in some meteorites. Here, we have carried out fine-scale mineralogical and microbial diversity analyses from surface and internal microbialite samples. Electron transmission microscopy revealed that the nanostructures correspond to rounded aragonite nanoprecipitates. A progressive mineralization of cells by the deposition of nanoprecipitates on their surface was observed from external towards internal microbialite areas. Molecular diversity studies based on 16S rDNA amplification revealed the presence of bacterial lineages affiliated to the Alpha-, Beta- and Gammaproteobacteria, the Cyanobacteria, the Cytophaga-Flexibacter-Bacteroides (CFB) group, the Actinobacteria and the Firmicutes. Cyanobacteria and CFB members were only detected in surface layers. The most abundant and diverse lineages were the Firmicutes (low GC Gram positives). To the exclusion of cyanobacteria, the closest cultivated members to the Lake Van phylotypes were most frequently alkaliphilic and/or heterotrophic bacteria able to degrade complex organics. These heterotrophic bacteria may play a crucial role in the formation of Lake Van microbialites by locally promoting carbonate precipitation.

Keywords

16S rRNA Aragonite Alkaliphile Biomineralization Electron microscopy Soda lake Phylogenetic analysis Stromatolite 

References

  1. Altermann W (2004) Precambrian stromatolites: problems in definition, classification, morphology and stratigraphy. In: Eriksson PG, Altermann W, Nelson DR, Mueller WU, Catuneanu O (eds) The Precambrian earth: tempos and events. Elsevier, Amsterdam, pp 564–574Google Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedGoogle Scholar
  3. Arp G, Reimer A, Reitner J (2001) Photosynthesis-induced biofilm calcification and calcium concentrations in Phanerozoic oceans. Science 292:1701–1704CrossRefPubMedGoogle Scholar
  4. Awramik SM (1971) Precambrian stromatolite diversity: reflection on metazoan appearance. Science 174:825–827Google Scholar
  5. Benzerara K, Menguy N, Guyot F, Dominici C, Gillet P (2003) Nanobacteria-like calcite single crystals at the surface of the Tataouine meteorite. Proc Natl Acad Sci USA 100:7438–7442CrossRefPubMedGoogle Scholar
  6. Burns BP, Goh F, Allen M, Neilan BA (2004) Microbial diversity of extant stromatolites in the hypersaline marine environment of Shark Bay, Australia. Environ Microbiol 6:1096–1101CrossRefPubMedGoogle Scholar
  7. Cao X, Liu X, Dong X (2003) Alkaliphilus crotonatoxidans sp. nov., a strictly anaerobic, crotonate-dismutating bacterium isolated from a methanogenic environment. Int J Syst Evol Microbiol 53:971–975Google Scholar
  8. Chafetz HS, Buczynski C (1992) Bacterially induced lithification of microbial mats. Palaios 7:277–293Google Scholar
  9. Dravis JJ (1983) Hardened subtidal stromatolites, Bahamas. Science 219:385–386Google Scholar
  10. Duckworth AW, Grant S, Grant WD, Jones BE, Meijer D (1998) Dietzia natronolimnaios sp. nov., a new member of the genus Dietzia isolated from an east African soda lake. Extremophiles 2:359–66Google Scholar
  11. Folk RL (1993) SEM imaging of bacteria and nannobacteria in carbonate sediments and rocks. J Sed Petrol 63:990–999Google Scholar
  12. Francis CA, Tebo BM (2002) Enzymatic manganese(II) oxidation by metabolically dormant spores of diverse Bacillus species. Appl Environ Microbiol 68:874–880CrossRefPubMedGoogle Scholar
  13. Francis CA, Casciotti KL, Tebo BM (2002) Localization of Mn(II)-oxidizing activity and the putative multicopper oxidase, MnxG, to the exosporium of the marine Bacillus sp. strain SG-1. Arch Microbiol 178:450–456CrossRefPubMedGoogle Scholar
  14. Grant WD (1992) Alkaline environments. In: Lederberg J (ed) Encyclopedia of Microbiology. Academic, London, pp 73–80Google Scholar
  15. Grant S, Grant WD, Jones BE, Kato C, Li L (1999) Novel archaeal phylotypes from an East African alkaline saltern. Extremophiles 3:139–45CrossRefPubMedGoogle Scholar
  16. Grotzinger JP (1990) Geochemical model for Proterozoic stromatolite decline. Amer J Sci 290-A:80–103Google Scholar
  17. Grotzinger JP, Knoll AH (1999) Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27:313–358CrossRefPubMedGoogle Scholar
  18. Hammes F, Boon N, de Villiers J, Verstraete W, Siciliano SD (2003) Strain-specific ureolytic microbial calcium carbonate precipitation. Appl Environ Microbiol 69:4901–4909CrossRefPubMedGoogle Scholar
  19. Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69:1030–1042CrossRefPubMedGoogle Scholar
  20. Jobb G (2002) TREEFINDER, Distributed by the author at http://www.treefinder.de
  21. Jones BE, Grant WD, Duckworth AW, Owenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2:191–200PubMedGoogle Scholar
  22. Kawaguchi T, Decho AW (2002) Isolation and biochemical characterization of extracellular polymeric secretions (EPS) from modern soft marine stromatolites (Bahamas) and its inhibitory effect on CaCO3 precipitation. Prep Biochem Biotechnol 32:51–63CrossRefPubMedGoogle Scholar
  23. Kazmierczak J, Kempe S (2003) Modern terrestrial analogues for the carbonate globules in Martian meteorite ALH84001. Naturwissenschaften 90:167–72PubMedGoogle Scholar
  24. Kazmierczak J, Kempe S, Altermann W (2004) Microbial origin of Precambrian carbonates: Lessons from modern analogues. In: Eriksson PG, Altermann W, Nelson DR, Mueller WU, Catuneanu O (eds) The Precambrian Earth: Tempos and Events. Elsevier, Amsterdam, pp 545–556Google Scholar
  25. Kempe S, Kazmierczak J (1990) Calcium carbonate supersaturation and the formation of in situ calcified stromatolites. In: Ittekott VA, Kempe S, Michaelis W, Spitzy A (eds) Facets of Modern Biogeochemistry. Springer, Berlin, pp 255–278Google Scholar
  26. Kempe S, Kazmierczak J (1993) Satonda Crater Lake, Indonesia: Hydrogeochemistry and biocarbonates. Facies 28:1–32Google Scholar
  27. Kempe S, Kazmierczak J (1994) The role of alkalinity in the evolution of ocean chemistry, organization of living systems, and biocalcification processes. In: Doumenge F, Allemand D, Toulemont A (eds), Past and present biomineralization processes. Considerations about the carbonate cycle, Inst Océanogr Bull, no spec 13: 61–117Google Scholar
  28. Kempe S, Kazmierczak J, Landmann G, Konuk T, Reimer A, Lipp A (1991) Largest known microbialites discovered in Lake Van, Turkey. Nature 349:605–608CrossRefGoogle Scholar
  29. Knorre H, Krumbein WE (2000) Bacterial calcification. In: Riding RE, Awramik SM (eds) Microbial sediments. Springer, Berlin, pp 25–31Google Scholar
  30. Krumbein WE (1979) Calcification by bacteria and algae. In: Trudinger PA, Swaine DJ (eds) Biogeochemical cycling of mineral-forming elements. Elsevier, Amsterdam, pp 47–68Google Scholar
  31. Lee YN (2003) Calcite production by Bacillus amyloquefaciens CMB01. J Microbiol 41:345–348Google Scholar
  32. Logan BW (1961) Cryptozoon and associated stromatolites from the Recent, Shark Bay, Western Australia. J Geol 69:517–533Google Scholar
  33. López-Archilla A, Moreira D, López-García P, Guerrero C (2004) Phytoplankton diversity and cyanobacterial dominance in a hypereutrophic shallow lake with biologically-produced alkaline pH. Extremophiles 8:109–115CrossRefPubMedGoogle Scholar
  34. Ma Y, Zhang W, Xue Y, Zhou P, Ventosa A, Grant WD (2004) Bacterial diversity of the Inner Mongolian Baer Soda Lake as revealed by 16S rRNA gene sequence analyses. Extremophiles 8:45–51CrossRefPubMedGoogle Scholar
  35. Marquis RE, Shin SY (1994) Mineralization and responses of bacterial spores to heat and oxidative agents. FEMS Microbiol Rev 14:375–379CrossRefPubMedGoogle Scholar
  36. Merz M (1992) The biology of carbonate precipitation by cyanobacteria. Facies 26:81–102Google Scholar
  37. Muliukin AL, Sorokin VV, Loiko NG, Suzina NE, Duda VI, Vorob’eva EA, El-Registan GI (2002) Comparative study of the elemental composition of vegetative and dormant microbial cells. Mikrobiologiia 71:37–48Google Scholar
  38. Neilan BA, Burns BP, Relman DA, Lowe DR (2002) Molecular identification of cyanobacteria associated with stromatolites from distinct geographical locations. Astrobiology 2:271–280Google Scholar
  39. Obst M, Sallam A, Luftmann H, Steinbuchel A (2004) Isolation and characterization of gram-positive cyanophycin-degrading bacteria-kinetic studies on cyanophycin depolymerase activity in aerobic bacteria. Biomacromolecules 5:153–161CrossRefPubMedGoogle Scholar
  40. Paerl HW, Pinckney JL, Steppe TF (2000) Cyanobacterial-bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments. Environ Microbiol 2:11–26Google Scholar
  41. Paerl HW, Steppe TF, Reid RP (2001) Bacterially mediated precipitation in marine stromatolites. Environ Microbiol 3:123–130Google Scholar
  42. Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  43. Pedone VA, Folk RL (1996) Formation of aragonite cement by nannobacteria in the Great Salt Lake, Utah. Geology 24:763–765CrossRefGoogle Scholar
  44. Pentecost A, Bauld J (1988) Nucleation of calcite on the sheaths of cyanobacteria using a simple diffusion cell. Geomicrobiol J 6:129–135Google Scholar
  45. Philippe H (1993) MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res 21:5264–5272PubMedGoogle Scholar
  46. Picossi S, Valladares A, Flores E, Herrero A (2004) Nitrogen-regulated genes for the metabolism of cyanophycin, a bacterial nitrogen reserve polymer: expression and mutational analysis of two cyanophycin synthetase and cyanophycinase gene clusters in heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. J Biol Chem 279:11582–11592CrossRefPubMedGoogle Scholar
  47. Rees HC, Grant WD, Jones BE, Heaphy S (2004) Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8:63–71CrossRefPubMedGoogle Scholar
  48. Reichenbach H (1999a) The Genus Lysobacter. In: Dworkin M (ed), The Prokaryotes: An evolving electronic resource for the microbiological community, Springer-Verlag, Berlin, p http://link.springer-ny.com/link/service/books/10125/
  49. Reichenbach H (1999b) The order Cytophagales. In Dworkin M (Ed), The Prokaryotes: An evolving electronic resource for the microbiological community, Springer-Verlag, http://link.springer-ny.com/link/service/books/10125/
  50. Reid RP, Browne KM (1991) Intertidal stromatolites in a fringing Holocene reef complex in the Bahamas. Geology 19:15–18CrossRefGoogle Scholar
  51. Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C, Macintyre IG, Paerl HW, Pinckney JL, Prufert-Bebout L, Steppe TF, DesMarais DJ (2000) The role of microbes in accretion, lamination and early lithification of modern marine stromatolites. Nature 406:989–992CrossRefPubMedGoogle Scholar
  52. Reid RP, James NP, Macintyre IG, Dupraz CP, Burne RV (2003) Shark Bay stromatolites: Microfabrics and reinterpretation of origins. Facies 49:45–53Google Scholar
  53. Riding R (1982) Cyanophyte calcification and changes in ocean chemistry. Nature 299:814–815CrossRefGoogle Scholar
  54. Rivadeneyra MA, Delgado G, Soriano M, Ramos-Cormenzana A, Delgado R (1999) Biomineralization of carbonates by Marinococcus albus and Marinococcus halophilus isolated from the Salar de Atacama (Chile). Curr Microbiol 39:53–57PubMedGoogle Scholar
  55. Rodriguez-Navarro C, Rodriguez-Gallego M, Ben Chekroun K, Gonzalez-Munoz MT (2003) Conservation of ornamental stone by Myxococcus xanthus-induced carbonate biomineralization. Appl Environ Microbiol 69:2182–2193CrossRefPubMedGoogle Scholar
  56. Stolz JF, Feinstein TN, Salsi J, Visscher PT, Reid RP (2001) TEM analysis of microbial mediated sedimentation and lithification in modern marine stromatolites. Am Mineral 86:826–833Google Scholar
  57. Stougaard P, Jorgensen F, Johnsen MG, Hansen OC (2002) Microbial diversity in ikaite tufa columns: an alkaline, cold ecological niche in Greenland. Environ Microbiol 4:487–493Google Scholar
  58. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  59. Visscher PT, Reid RP, Bebout BM, Hoeft SE, Macintyre IG, Thompson JA (1998) Formation of lithified micritic laminae in modern marine stromatolites (Bahamas): The role of sulfur cycling. Am Mineral 83:1482–1493Google Scholar
  60. Visscher PT, Reid PR, Bebout BM (2000) Microscale observations of sulfate reduction: Correlation of microbial activity with lithified micritic laminae in modern marine stromatolites. Geology 28:919–922Google Scholar
  61. Walter MR (1983) Archaean stromatolites: evidence of Earth’s earliest benthos. In: Schopf JW (ed) Earth’s earliest biosphere, its origin and evolution. Princeton University Press, Princeton, pp 187–213Google Scholar
  62. Walter MR, Heys GR (1985) Links between the rise of metazoa and the decline of stromatolites. Precambr Res 29:149–174CrossRefGoogle Scholar
  63. Yi H, Chun J (2004) Hongiella mannitolivorans gen. nov., sp. nov., Hongiella halophila sp. nov. and Hongiella ornithinivorans sp. nov., isolated from tidal flat sediment. Int J Syst Evol Microbiol 54:157–162Google Scholar
  64. Yumoto I, Nakamura A, Iwata H, Kojima K, Kusumoto K, Nodasaka Y, Matsuyama H (2002) Dietzia psychralcaliphila sp. nov., a novel, facultatively psychrophilic alkaliphile that grows on hydrocarbons. Int J Syst Evol Microbiol 52:85–90Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Purificación López-García
    • 1
  • Józef Kazmierczak
    • 2
  • Karim Benzerara
    • 3
    • 5
  • Stephan Kempe
    • 4
  • François Guyot
    • 3
  • David Moreira
    • 1
  1. 1.Unité d’Ecologie, Systématique et Evolution, UMR CNRS 8079Université Paris-SudOrsay CedexFrance
  2. 2.Institute of PaleobiologyPolish Academy of SciencesWarsawPoland
  3. 3.Laboratoire de Minéralogie-CristallographieUMR 7590 CNRS and Institut de Physique du Globe de ParisParis CedexFrance
  4. 4.Institut für Angewandte GeowissenschaftenTechnische Universität DarmstadtDarmstadtGermany
  5. 5.Surface & Aqueous Geochemistry Group, Department of Geological and Environmental SciencesStanford UniversityStanfordUSA

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