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Microbial Ecology

, Volume 59, Issue 4, pp 689–699 | Cite as

Endolithic Microbial Colonization of Limestone in a High-altitude Arid Environment

  • Fiona K. Y. Wong
  • Maggie C. Y. Lau
  • Donnabella C. Lacap
  • Jonathan C. Aitchison
  • Donald A. Cowan
  • Stephen B. PointingEmail author
Environmental Microbiology

Abstract

The morphology of endolithic colonization in a limestone escarpment and surrounding rocky debris (termed float) at a high-altitude arid site in central Tibet was documented using scanning electron microscopy. Putative lichenized structures and extensive coccoid bacterial colonization were observed. Absolute and relative abundance of rRNA gene signatures using real-time quantitative polymerase chain reaction and phylogenetic analysis of environmental phylotypes were used to characterize community structure across all domains. Escarpment endoliths were dominated by eukaryotic phylotypes suggestive of lichenised associations (a Trebouxia lichen phycobiont and Leptodontidium lichen mycobiont), whereas float endoliths were dominated by bacterial phylotypes, including the cyanobacterium Chroococcidiopsis plus several unidentified beta proteobacteria and crenarchaea. Among a range of abiotic variables tested, ultraviolet (UV) transmittance by rock substrates was the factor best able to explain differences in community structure, with eukaryotic lichen phylotypes more abundant under conditions of greater UV-exposure compared to prokaryotes. Variously pigmented float rocks did not support significantly different communities. Estimates of in situ carbon fixation based upon 14C radio-labelled bicarbonate uptake indicated endolithic productivity of approximately 2.01 g C/m2/year−1, intermediate between estimates for Antarctic and temperate communities.

Keywords

Photosynthetically Active Radiation Archaea Solar Noon Bacterial Phylotypes Float Rock 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors are grateful to the Tibet Ministry of Geology for fieldwork assistance and to the Hong Kong Research Grants Council (grant numbers HKU 7375/05M and HKU 7733/08M) and Stephen Hui Trust Fund for financial support.

Supplementary material

248_2009_9607_MOESM1_ESM.doc (849 kb)
Fig. S1 Denaturing gradient gel electrophoresis (DGGE) profiles for limestone endolithon (scarp, gray float [GF], pink float [PF], white float [WF], pink layer [PL], and green layer [GL]) using polymerase chain reaction primers specific to eukarya (a), bacteria (b), cyanobacteria (c), and archaea (d). Numbers beside each gel indicate the denaturant gradient, numbers specific to each band are the phylotype identifiers (same as used in phylogenetic trees), asterisks in bacteria DGGE indicate plastid phylotypes, white arrows in bacteria DGGE (b) indicate cyanobacterial phylotypes and white arrows in eukaryal DGGE (a) indicate fungal phylotypes. (DOC 849 kb)
248_2009_9607_MOESM2_ESM.doc (104 kb)
Table S1 Abiotic variables for limestone scarp and float colonized by endolithic microorganisms. (DOC 104 kb)

References

  1. 1.
    Billi D, Friedmann EI, Hofer K, Grilli-Caiola M, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489CrossRefPubMedGoogle Scholar
  2. 2.
    Budel B, Webber B, Kuhl M, Pfanz H, Sultemeyer D, Wessels D (2004) Reshaping of sandstone surfaces by cryptoendolithic cyanobacteria: bioalkalization causes chemical weathering in arid landscapes. Geobiology 2:261CrossRefGoogle Scholar
  3. 3.
    Cockell CS, Stokes MD (2004) Widespread colonization by polar hypoliths. Nature 431:414CrossRefPubMedGoogle Scholar
  4. 4.
    de la Torre JR, Goebel BR, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo dry valleys, Antarctica. Appl Environ Microbiol 69:3858CrossRefPubMedGoogle Scholar
  5. 5.
    Edwards HGM, Cockell CS, Newton ES, Wynn-Williams DD (2004) Protective pigmentation in UV-B-screened Antarctic lichens studied by Fourier transform Raman spectroscopy: an extremophile bioresponse to radiation stress. J Raman Spectrosc 35:463CrossRefGoogle Scholar
  6. 6.
    Friedmann EI (1980) Endolithic microbial life in hot and cold deserts. Orig Life Evol Biosph 10:223CrossRefGoogle Scholar
  7. 7.
    Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:1045CrossRefPubMedGoogle Scholar
  8. 8.
    Friedmann EI, KAppen L, Meyer MA, Nienow JA (1993) Long-term productivity in the cryptoendolithic microbial community of the Ross desert, Antarctica. Microb Ecol 25:51CrossRefPubMedGoogle Scholar
  9. 9.
    Friedmann EI, Ocampo R (1976) Endolithic blue-green algae in dry valleys—primary producers in Antarctic desert ecosystem. Science 193:1247CrossRefPubMedGoogle Scholar
  10. 10.
    Gerrath JA, Mathes U, Larson DW (2000) Endolithic algae and cyanobacteria from cliffs of the Niagara Escarpment, Ontario, Canada. Can J Bot 78:807CrossRefGoogle Scholar
  11. 11.
    Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765PubMedGoogle Scholar
  12. 12.
    Kuhle M (1990) The cold deserts of high Asia (Tibet and contiguous mountains). GeoJournal 20:319CrossRefGoogle Scholar
  13. 13.
    Lau CY, Jing H, Aitchison JC, Pointing SB (2006) Highly diverse community structure in a remote central Tibetan geothermal spring does not display monotonic variation to thermal stress. FEMS Microbiol Ecol 57:80CrossRefGoogle Scholar
  14. 14.
    Mathes-Sears U, Gerrath JA, Larson DW (1997) Abundance, biomass and productivity of endolithic and epilithic lower plants on the temperate-zone cliffs of the Niagara Escarpment, Canada. Int J Plant Sci 158:451CrossRefGoogle Scholar
  15. 15.
    McKay CP (1993) Relevance of Antarctic microbial ecosystems to exobiology. In: Friedmann EI (ed) Antarctic microbiology. Wiley-Liss, New York, p 593Google Scholar
  16. 16.
    Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695PubMedGoogle Scholar
  17. 17.
    Norris T, Castenholz RW (2006) Endolithic photosynthetic communities within ancient and recent travertine deposits in Yellowstone national Park. FEMS Microbiol Ecol 57:470CrossRefPubMedGoogle Scholar
  18. 18.
    Pointing SB, Chan Y, Lacap DC, Lau CY, Jurgens J, Farrell RL (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA (in press)Google Scholar
  19. 19.
    Pointing SB, Chan Y, Lacap DC, Lau CY, Jurgens J and Farrell RL (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci (USA). doi: 10.1073/pnas.0908274106
  20. 20.
    Rannala B, Yang ZH (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. Mol Ecol 43:304Google Scholar
  21. 21.
    Sanchoz LG, de la Torre R, Horneck G, Ascaso C, de los Rios A, Pintado A, Wierzchos J, Schuster M (2007) Lichens in space: results from the 2005 LICHENS experiment. Astrobiology 7:443CrossRefGoogle Scholar
  22. 22.
    Sigler WV, Bachofen R, Zeyer J (2003) Molecular characterization of endolithic cyanobacteria inhabiting exposed dolomite in central Switzerland. Environ Microbiol 5:618CrossRefPubMedGoogle Scholar
  23. 23.
    Sun HJ, Friedmann EI (1999) Growth on geological time scales in the Antarctic cryptoendolithic microbial community. Geomicrobiol J 16:193CrossRefGoogle Scholar
  24. 24.
    Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (*and other methods) version 4.0b8. Sinauer Associates, SunderlandGoogle Scholar
  25. 25.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876CrossRefGoogle Scholar
  26. 26.
    Walker JJ, Pace NR (2007) Phylogenetic composition of Rocky Mountain endolithic microbial ecosystems. Appl Environ Microbiol 73:3497CrossRefPubMedGoogle Scholar
  27. 27.
    Warren-Rhodes K, Rhodes KL, Pointing SB, Boyle L, Dungan J, Liu S, Zhou P, McKay CP (2007) Lithic cyanobacterial ecology across environmental gradients and spatial scales in China’s hot and cold deserts. FEMS Microbiol Ecol 61:470CrossRefPubMedGoogle Scholar
  28. 28.
    Warren-Rhodes K, Rhodes KL, Pointing SB, Ewing S, Lacap DC, Gómez-Silva B, Amundson R, Friedmann EI, McKay CP (2006) Hypolithic cyanobacteria, dry limit of photosynthesis and microbial ecology in the hyperarid Atacama Desert, Chile. Microb Ecol 52:389CrossRefPubMedGoogle Scholar
  29. 29.
    White TJ, Burns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Gelfand DH, Sninsky JJ, White TJ, Innis A (eds) PCR protocols, a guide to methods and applications. Academic, San Diego, p 315Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Fiona K. Y. Wong
    • 1
  • Maggie C. Y. Lau
    • 1
  • Donnabella C. Lacap
    • 1
  • Jonathan C. Aitchison
    • 2
  • Donald A. Cowan
    • 3
  • Stephen B. Pointing
    • 1
    Email author
  1. 1.School of Biological SciencesThe University of Hong KongHong KongPeople’s Republic of China
  2. 2.Department of Earth SciencesThe University of Hong KongHong KongPeople’s Republic of China
  3. 3.Institute for Microbial Biotechnology and MetagenomicsUniversity of the Western CapeCape TownSouth Africa

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