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

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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.

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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.

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Authors and Affiliations

  1. NASA-Ames Research Center, MS 245-3, Moffett Field, CA, 94035, USA

    Kimberley A. Warren-Rhodes, E. Imre Friedmann & Christopher P. McKay

  2. Department of Environmental Science, Policy and Management, Ecosystem Sciences Division, The University of California at Berkeley, Berkeley, CA, 94720, USA

    Kimberley A. Warren-Rhodes, Stephanie A. Ewing & Ronald Amundson

  3. Department of Agriculture, Forestry and Natural Resource Management, The University of Hawaii at Hilo, Hilo, HI, 96720, USA

    Kevin L. Rhodes

  4. Department of Ecology and Biodiversity, The University of Hong Kong, Pokfulam Road, Hong Kong SAR, China

    Stephen B. Pointing & Donnabella C. Lacap

  5. Departmento de Biomédico and Instituto del Desierto, Universidad de Antofagasta, Antofagasta, Chile

    Benito Gómez-Silva

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  1. Kimberley A. Warren-Rhodes
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Correspondence to Kimberley A. Warren-Rhodes.

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Warren-Rhodes, K.A., Rhodes, K.L., Pointing, S.B. et al. Hypolithic Cyanobacteria, Dry Limit of Photosynthesis, and Microbial Ecology in the Hyperarid Atacama Desert. Microb Ecol 52, 389–398 (2006). https://doi.org/10.1007/s00248-006-9055-7

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