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Microbial Ecology

, Volume 52, Issue 3, pp 389–398 | Cite as

Hypolithic Cyanobacteria, Dry Limit of Photosynthesis, and Microbial Ecology in the Hyperarid Atacama Desert

  • Kimberley A. Warren-Rhodes
  • Kevin L. Rhodes
  • Stephen B. Pointing
  • Stephanie A. Ewing
  • Donnabella C. Lacap
  • Benito Gómez-Silva
  • Ronald Amundson
  • E. Imre Friedmann
  • Christopher P. McKay
Article

Abstract

The occurrence of hypolithic cyanobacteria colonizing translucent stones was quantified along the aridity gradient in the Atacama Desert in Chile, from less arid areas to the hyperarid core where photosynthetic life and thus primary production reach their limits. As mean rainfall declines from 21 to ≤2 mm year−1, the abundance of hypolithic cyanobacteria drops from 28 to <0.1%, molecular diversity declines threefold, and organic carbon residence times increase by three orders of magnitude. Communities contained a single Chroococcidiopsis morphospecies with heterotrophic associates, yet molecular analysis revealed that each stone supported a number of unique 16S rRNA gene-defined genotypes. A fivefold increase in steady-state residence times for organic carbon within communities in the hyperarid core (3200 years turnover time) indicates a significant decline in biological carbon cycling. Six years of microclimate data suggest that the dry limit corresponds to ≤5 mm year−1 rainfall and/or decadal periods of no rain, with <75 h year−1 of liquid water available to cyanobacteria under light conditions suitable for photosynthesis. In the hyperarid core, hypolithic cyanobacteria are rare and exist in small spatially isolated islands amidst a microbially depauperate bare soil. These findings suggest that photosynthetic life is extremely unlikely on the present-day surface of Mars, but may have existed in the past. If so, such microhabitats would probably be widely dispersed, difficult to detect, and millimeters away from virtually lifeless surroundings.

Keywords

Liquid Water Rocky Desert Cyanobacterial Community Percent Colonization Aridity Gradient 
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

Acknowledgments

We thank C. Latorre for historical climate data, L. Cáceres for field assistance, Michaele Kashgarian and Paula Zermeno at the Center for Accelerator Mass Spectrometry and the University of California Agricultural Experimental Station, and three anonymous reviewers for their comments on the manuscript. We acknowledge support from NASA's Astrobiology Science and Technology for Exploring Planets Program, the National Academy of Sciences, National Research Council (KWR), NASA GSRP fellowship (SAE), and PROIM 1337-1 Universidad de Antofagasta.

References

  1. 1.
    Andrew, N, Mapstone, B (1987) Sampling and the description of spatial pattern in marine ecology. Oceanogr Mar Biol Ann Rev 25: 39–90Google Scholar
  2. 2.
    Arroyo, MT, Squeo, G, Armesto, J, Villagrán, C (1988) Effects of aridity on plant diversity in the Northern Chilean Andes: Results of a natural experiment. Ann Mo Bot Gard 75: 55–78CrossRefGoogle Scholar
  3. 3.
    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: 1489–1492PubMedCrossRefGoogle Scholar
  4. 4.
    Bonani, G, Friedmann, EI, Ocampo-Friedmann, R, McKay, CP, Woelfli, W (1988) Preliminary report on radiocarbon dating of cryptoendolithic microorganisms. Polarforschung 58: 199–200PubMedGoogle Scholar
  5. 5.
    Caasamayor, EO, Schafer, H, Baneras, L, Pedros-Alio, C, Muyzer, G (2002) Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microbiol 66: 499–508CrossRefGoogle Scholar
  6. 6.
    Cockell, C, Osinski, G, Lee, P (2003) The impact crater as a habitat: effects of impact processing of target materials. Astrobiology 3: 181–191PubMedCrossRefGoogle Scholar
  7. 7.
    Erickson, GE (1983) The Chilean nitrate deposits. Am Sci 71: 366–374Google Scholar
  8. 8.
    Friedmann, EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215: 1045–1053CrossRefPubMedGoogle Scholar
  9. 9.
    Friedmann, EI, Galun, M (1974) Desert algae, lichens and fungi. In: Brown, G (Ed.) Desert Biology. Academic Press, New York, pp 165–212Google Scholar
  10. 10.
    Friedmann, EI, Ocampo-Friedmann, R (1985) Blue-green algae in arid cryptoendolithic habitats. Arch Hydrobiol Suppl 71(1/2): 349–350Google Scholar
  11. 11.
    Friedmann, EI, Lipkin, Y, Ocampo-Paus, R (1967) Desert algae of the Negev (Israel). Phycologia 6: 185–196Google Scholar
  12. 12.
    Friedmann, EI, Druk, AY, McKay, CP (1994) Limits of life and microbial extinction in the Antarctic desert. Antarc J US 29: 176–179Google Scholar
  13. 13.
    Garcia-Pichel, F, Lopez-Cortes, A, Nubel, U (2001) Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado plateau. Appl Environ Microbiol 67: 1902–1910PubMedCrossRefGoogle Scholar
  14. 14.
    Grilli-Caiola, M, Ocampo-Friedmann, R, Friedmann, EI (1993) Cytology of long-term dessication in the desert cyanobacterium Chroococcidiopsis (Chroococcales). Phycologia 32: 315–322Google Scholar
  15. 15.
    Golubic, S, Friedmann, EI, Schneider, J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Petrol 51: 475–478Google Scholar
  16. 16.
    Haberle, R, McKay, C, Schaeffer, J, Cabrol, N, Grin, E, Zent, A, Quinn, R (2001) On the possibility of liquid water on present-day Mars. J Geophys Res 106: 23317–23326CrossRefGoogle Scholar
  17. 17.
    Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98Google Scholar
  18. 18.
    Hartley, A, Chong, G (2002) Late Pliocene age for the Atacama Desert: implications for the desertification of western South America. Geology 30: 43–46CrossRefGoogle Scholar
  19. 19.
    Hecht, M (2002) Metastability of liquid water on Mars. Icarus 156: 373–386CrossRefGoogle Scholar
  20. 20.
    Houston, J, Hartley, A (2003) The central Andean west-slope rainshadow and its potential contribution to the origin of hyper-aridity in the Atacama Desert. Int J Climatol 23: 1453–1464CrossRefGoogle Scholar
  21. 21.
    Krebs, C (1989) Ecological Methodology. Harper and Row, CambridgeGoogle Scholar
  22. 22.
    Lane, DJ, Pace, B, Olsen, GJ, Stahl, DA, Sogin, ML, Pace, NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82: 6955–6959PubMedCrossRefGoogle Scholar
  23. 23.
    Larrain, H, Velásquez, Cereceda, P, Espejo, R, Pinto, R, Osses, P, Schemenauer, RS (2002) Fog measurements at the site “Falda Verde” north of Chañaral with other fog stations of Chile. Atmos Res 64: 273–284CrossRefGoogle Scholar
  24. 24.
    Latorre, C (2002) Clima y Vegetación del Desierto de Atacama Durante el Cuaternario Tardío, II Región, Chile. Ph.D. dissertation, Universidad de Chile, SantiagoGoogle Scholar
  25. 25.
    Lobitz, B, Wood, B, Averner, M, McKay, CP (2001) Use of spacecraft data to derive regions on Mars where liquid water would be stable. Proc Natl Acad Sci USA 98: 2132–2137PubMedCrossRefGoogle Scholar
  26. 26.
    McKay, CP, Long, A, Friedmann, EI (1986) Radiocarbon dating of open systems with bomb effect. J Geophys Res 91: 3836–3840Google Scholar
  27. 27.
    McKay, CP, Friedmann, EI, Gómez-Silva, B, Cáceres, L, Andersen, D, Landheim, R (2003) Temperature and moisture conditions in the extreme arid regions of the Atacama Desert: four years of observations including the El Niño of 1997–1998. Astrobiology 3: 393–406PubMedCrossRefGoogle Scholar
  28. 28.
    Miller, A (1976) The climate of Chile. In: Schwerdtfeger, R (Ed.) World Survey of Climatology. Vol. 12: Climates of Central and South America, Elsevier Scientific Publishing Company, Amsterdam, pp 113–145Google Scholar
  29. 29.
    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: 695–700PubMedGoogle Scholar
  30. 30.
    Navarro-González, R, Rainey, F, Molina, P, Bagaley, D, Hollen, B, de la Rosa, J, Small, A, Quinn, R, Cáceres, L, Gomez-Silva, B, McKay, CP (2003) Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science 302: 933–1096CrossRefGoogle Scholar
  31. 31.
    Nienow, J, Friedmann, EI (1993) Terrestrial lithophytic (rock) communities. In: Friedmann, EI (Ed.) Antarctic Microbiology, Wiley-Liss, New York, pp 243–412Google Scholar
  32. 32.
    Owen, JK, Nishiizumi, K, Sharp, W, Sutter, B, Ewing, S, Amundson, R (2003) Investigations into the numerical ages of post-Miocene fluvial landforms in the Atacama Desert, Chile. Eos Trans. AGU 84(46), Fall Meet. Suppl. Abstract T31CGoogle Scholar
  33. 33.
    Potts, M, Friedmann, EI (1981) Effects of water stress on cryptoendolithic cyanobacteria from hot desert rocks. Arch Microbiol 130: 267–271CrossRefGoogle Scholar
  34. 34.
    Rannala, B, Yang, ZH (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Ecol 43: 304–311Google Scholar
  35. 35.
    Rech, J, Quade, J, Hart, W (2003) Isotopic evidence for the source of Ca and S in soil gypsum, anhydrite and calcite in the Atacama Desert, Chile. Geochim Cosmochim Acta 67: 575–586CrossRefGoogle Scholar
  36. 36.
    Reider, R, Gellert, R, Anderson, RC, Brückner, J, Clark, BC, Dreibus, G, Economou, T, Klingelhöfer, G, Lugmair, G, Ming, D, Squyres, S, d'Uston, C, Wänke, H, Yen, A, Zipfel, J (2004) Chemistry of rocks and soils at Meridiani Planum from the alpha particle X-ray spectrometer. Science 306: 1746–1749CrossRefGoogle Scholar
  37. 37.
    Rietkerk, M, Dekker, S, Ruiter, P, van de Koppel, J (2004) Self-organized patchiness and catastrophic shifts in ecosystems. Science 305: 1926–1929PubMedCrossRefGoogle Scholar
  38. 38.
    Rundel, P, Dillon, M, Palma, B, Mooney, H, Gulman, S, Ehleringer, J (1991) The phytogeography and ecology of the coastal Atacama and Peruvian deserts. Aliso 13: 1–49Google Scholar
  39. 39.
    Schafer, H, Muyzer, G (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. Methods Microbiol 30: 425–468Google Scholar
  40. 40.
    Schlesinger, WH, Reynolds, J, Cunningham, G, Huenneke, L, Jarrell, W, Virginia, R, Whitford, W (1990) Biological feedbacks in global desertification. Science 247: 1043–1048CrossRefPubMedGoogle Scholar
  41. 41.
    Schlesinger, WH, Pippin, J, Wallenstein, M, Hofmockel, K, Klepeis, D, Hahall, B (2003) Community composition and photosynthesis by photoautotrophs under quartz pebbles, southern Mojave Desert. Ecology 84: 3222–3231Google Scholar
  42. 42.
    Stuiver, M, Polach, HA (1977) Reporting of C-14 data—discussion. Radiocarbon 19: 355–363Google Scholar
  43. 43.
    Swofford, DL (2001) PAUP*: Phylogenetic analysis using parsimony (*and other methods) version 4.0b8. Sinauer Associates, SunderlandGoogle Scholar
  44. 44.
    Villagrán, C, Arroyo, M, Marticorena, C (1983) Efectos de la desertización en la distribución de la flora andina de Chile. Rev Chil Hist Nat 56: 137–157Google Scholar
  45. 45.
    Vogel, S (1955) Niedere “Fensterpflanzen” in der südafrikanischen Wüste. Beitr Biol Pflanz 31: 45–135Google Scholar
  46. 46.
    Wang, Y, Amundson, R, Trumbore, S (1996) Radiocarbon dating of soil organic matter. Quat Res 45: 282–288CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Kimberley A. Warren-Rhodes
    • 1
    • 2
  • Kevin L. Rhodes
    • 3
  • Stephen B. Pointing
    • 4
  • Stephanie A. Ewing
    • 2
  • Donnabella C. Lacap
    • 4
  • Benito Gómez-Silva
    • 5
  • Ronald Amundson
    • 2
  • E. Imre Friedmann
    • 1
  • Christopher P. McKay
    • 1
  1. 1.NASA-Ames Research CenterMoffett FieldUSA
  2. 2.Department of Environmental Science, Policy and Management, Ecosystem Sciences DivisionThe University of California at BerkeleyBerkeleyUSA
  3. 3.Department of Agriculture, Forestry and Natural Resource ManagementThe University of Hawaii at HiloHiloUSA
  4. 4.Department of Ecology and BiodiversityThe University of Hong KongHong Kong SARChina
  5. 5.Departmento de Biomédico and Instituto del DesiertoUniversidad de AntofagastaAntofagastaChile

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