Skip to main content Accessibility help

Rapid colonization of artificial endolithic uninhabited habitats

  • Charles S. Cockell (a1), Luke Hecht (a1), Hanna Landenmark (a1), Samuel J. Payler (a1) and Matthew Snape (a1)...


To test the rate at which a lifeless but habitable environment (uninhabited habitat) can be colonized, artificial endolithic habitats were constructed in the laboratory and exposed to the natural environment. They were composed of sterile stacked sintered glass discs (stacks) containing CHNOPS elements, liquid water, energy and a carbon source, making them habitable for aerobic respiring organisms and phototrophs. One set of stacks was exposed fully to atmospheric conditions and one set was covered from direct overhead atmospheric input and precipitation. The process of colonization was heterogeneous across the stacks. After 3 months, all uninhabited habitats were colonized at all depths in both fully exposed and covered stacks. However, uninhabited habitable conditions persisted in covered stacks after 1 month, demonstrating the importance of the hydrological cycle in the connection between inhabited habitats and uninhabited habitats. Low porosity rocks were found to retard the extent of colonization compared with higher porosity rocks. Examination of genomic DNA demonstrated that the habitats were colonized by a community dominated by Proteobacteria. Covered stacks had a higher abundance of fungal sequences among eukaryotic colonizers. These data demonstrate the tight coupling between the appearance of habitable conditions and life and the reasons for the rarity of uninhabited habitats on the present-day Earth. On other planetary bodies, such as Mars, with more inclement atmospheres and less vigorous hydrological cycles or a lack of life, uninhabited habitats could persist for longer with consequences for the interpretation of data sent back by planetary science missions.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Rapid colonization of artificial endolithic uninhabited habitats
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Rapid colonization of artificial endolithic uninhabited habitats
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Rapid colonization of artificial endolithic uninhabited habitats
      Available formats


This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (, which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: Charles S. Cockell, E-mail:


Hide All
Abu-Ashour, J, Joy, DM, Lee, H, Whiteley, HR and Zelin, S (1994) Transport of microorganisms through soil. Water, Air and Soil Pollution 75, 141158.
Amman, RI, Ludwig, W and Schleifer, K-H. (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiology Reviews 59, 143169.
Bowers, RM, Clements, N, Emerson, JB, Wiedinmyer, C, Hannigan, MP and Fierer, N (2013) Seasonal variability in bacterial and fungal diversity of the near-surface atmosphere. Environmental Science and Technology 47, 1209712106.
Brock, TD (1973) Primary colonization of Surtsey, with special reference to the blue-green algae. Oikos 24, 239243.
Caporaso, JG, Kuczynski, J, Stombaugh, J, Bittinger, K, Bushman, FD, Costello, EK, Fierer, N, Pena, AG, Goodrich, JK, Gordon, JI and Huttley, GA (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335336.
Chapin, FS, Walker, LR, Fastie, CL and Sharman, LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecological Monographs 64, 149175.
Cockell, CS (2011) Vacant habitats in the Universe. Trends in Ecology and Evolution 26, 7380.
Cockell, CS (2014) Types of habitat in the Universe. International Journal of Astrobiology 13, 158164.
Cockell, CS, Balme, M, Bridges, JC, Davila, A and Schwenzer, SP (2012) Uninhabited habitats on Mars. Icarus 217, 184193.
Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 24602461.
Edgar, RC (2011) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10, 996998.
Edgar, RC, Haas, BJ, Clemente, JC, Quince, C and Knight, R (2013) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 21942200.
Elbert, W, Taylor, PE, Andreae, MO and Pöschl, U (2007) Contribution of fungi to primary biogenic aerosols in the atmosphere: wet and dry discharged spores, carbohydrates, and inorganic ions. Atmospheric Chemistry and Physics 7, 45694588.
Evans, CA, Coombes, PJ and Dunstan, RH (2006) Coliforms, biofilms, microbial diversity and the quality of roof-harvested rainwater. Wind, rain and bacteria: the effect of weather on the microbial composition of roof-harvested rainwater. Water Research 40, 3744.
Field, CB, Behrenfeld, MJ, Randerson, JT and Falkowski, P (1998) Primary production in the biosphere: integrating terrestrial and oceanic components. Science 281, 237240.
Friedmann, EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215, 10451053.
Gomez-Alvarez, V, King, GM and Nüsslein, K (2007) Comparative bacterial diversity in recent Hawaiian volcanic deposits of different ages. FEMS Microbiology Ecology 60, 6073.
Grant, CL and Pramer, D (1962) Minor element composition of yeast extract. Journal of Bacteriology 84, 869870.
Grotzinger, JP, Sumner, DY, Kah, LC, Stack, K, Gupta, S, Edgar, L, Rubin, D, Lewis, K, Schieber, J, Mangold, N, Milliken, R, Conrad, PG, DesMarais, D, Farmer, J, Siebach, K, Calef, F, Hurowitz, J, McLennan, SM, Ming, D, Vaniman, D, Crisp, J, Vasavada, A, Edgett, KS, Malin, M, Blake, D, Geliert, R, Mahaffy, P, Wiens, RC, Maurice, S, Grant, JA, Wilson, S, Anderson, RC, Beegle, L, Arvidson, R, Hallet, B, Sletten, RS, Rice, M, Bell, J, Griffes, J, Ehlmann, B, Anderson, RB, Bristow, TF, Dietrich, WE, Dromart, G, Eigenbrode, J, Fraeman, A, Hardgrove, C, Herkenhoff, K, Jandura, L, Kocurek, G, Lee, S, Leshin, LA, Leveille, R, Limonadi, D, Maki, J, McCloskey, S, Meyer, M, Minitti, M, Newsom, H, Oehler, D, Okon, A, Palucis, M, Parker, T, Rowland, S, Schmidt, M, Squyres, S, Steele, A, Stolper, E, Summons, R, Treiman, A, Williams, R, Yingst, A and MSL Science Team (2013) A habitable fluvio-lacustrine environment at Yellowknife Bay, Gale Crater, Mars. Science 343, 1242777. doi: 10.1126/science.1242777.
Huffman, JA, Prenni, AJ, DeMott, PJ, Pöhlker, C, Mason, RH, Robinson, NH, Fröhlich-Nowoisky, J, Tobo, Y, Després, VR, Garcia, E, Gochis, DJ, Harris, E, Müller-Germann, I, Ruzene, C, Schmer, B, Sinha, B, Day, DA, Andreae, MO, Jiminez, JL, Gallagher, M, Kreidenweis, SM, Bertram, AK and Pöschl, U (2013) High concentrations of biological aerosol particles and ice nuclei during and after rain. Atmospheric Chemistry and Physics 13, 61516164.
Huysman, E and Verstraete, W (1993) Water-facilitated transport of bacteria in unsaturated soil columns: influence of cell surface hydrophobicity and soil properties. Soil Biology and Biochemistry 25, 8390.
Ibekwe, MA, Kennedy, AC, Halvorson, JJ and Yang, C-H (2007) Characterization of developing microbial communities in Mount St. Helens pyroclastic substrate. Soil Biology and Biochemistry 39, 24962507.
Kelly, LC, Cockell, CS, Thorsteinsson, T, Marteinsson, V and Stevenson, J (2014) Pioneer microbial communities of the Fimmvörðuháls Lava Flow, Eyjafjallajökull, Iceland. Microbial Ecology 68, 504518.
Krone, RB, Orlob, GT and Hodgkinson, C (1958) Movement of coliform bacteria through porous media. Sewage and Industrial Wastes 30, 113.
Martins, Z, Botta, O, Fogel, ML, Sephton, MA, Glavin, DP, Watson, JS, Dworkin, JP, Schwartz, AW and Ehrenfreund, P (2008) Extraterrestrial nucleobases in the Murchison meteorite. Earth and Planetary Science Letters 270, 130136.
Mautner, MN (2002) Planetary bioresources and astroecology 1. Planetary microcosm bioassays of Martian and carbonaceous chondrite materials: nutrients, electrolyte solutions, and algal and plant responses. Icarus 158, 7286.
Nemergut, D, Anderson, S, Cleveland, C, Martin, A, Miller, A, Seimon, A and Schmidt, SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microbial Ecology 53, 110122.
Odum, E (1971) Fundamentals of Ecology. Saunders, Philadelphia PA
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590D596.
Raven, JA (2009) Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquatic Microbial Ecology 56, 177192.
Rippka, R, Deruelles, J, Waterbury, JB, Herdman, M and Stanier, RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111, 161.
Schütte, UME, Abdo, Z, Foster, J, Ravel, J, Bunge, J, Solheim, B and Forney, LJ (2010) Bacterial diversity in a glacier foreland of the high Arctic. Molecular Ecology 19, 5466.
Seifried, JS, Wichels, A and Gerdts, G (2015) Spatial distribution of marine airborne bacterial communities. MicrobiologyOpen 4, 475490. doi: 10.1002/mbo3.253.
Sephton, MA (2002) Organic compounds in carbonaceous meteorites. Natural Product Reports 19, 292311.
Staley, JT and Konopka, A (1985) Measurements of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annual Reviews of Microbiology 39, 321346.
Vaitilingom, M, Deguillaume, L, Vinatier, V, Sancelme, M, Amato, P, Chaumerliac, N and Delort, AM (2013) Potential impact of microbial activity on the oxidant capacity and organic carbon budget in clouds. Proceedings of the National Academy of Sciences of the United States of America 110, 559564.
van Elsas, JD, Trevors, JT and van Overbeek, LS (1991) Influence of soil properties on the vertical movement of genetically-marked Pseudomonas fluorescens through large soil microcosms. Biology and Fertility of Soils 10, 249255.
Wolf, AB, Vos, M, de Boer, W and Kowalchuk, GA (2013) Impact of matric potential and pore size distribution on growth dynamics of filamentous and non-filamentous soil bacteria. PLoS ONE 8, e83661.
Womack, AM, Bohannan, BJM and Green, JL (2010) Biodiversity and biogeography of the atmosphere. Philosophical Transactions of the Royal Society B 365, 36453653.


Related content

Powered by UNSILO

Rapid colonization of artificial endolithic uninhabited habitats

  • Charles S. Cockell (a1), Luke Hecht (a1), Hanna Landenmark (a1), Samuel J. Payler (a1) and Matthew Snape (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.