Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-24T01:16:42.866Z Has data issue: false hasContentIssue false
  • English
  • Français

Are thermophilic microorganisms active in cold environments?

Published online by Cambridge University Press:  10 November 2014

Charles S. Cockell ,
Claire Cousins ,
Paul T. Wilkinson ,
Karen Olsson-Francis  and
Ben Rozitis
Charles S. Cockell*
Affiliation:
UK Centre for Astrobiology, School of Physics and Astronomy, University of Edinburgh, Edinburgh EH9 3JZ, UK Department of Physical Science, Centre for Earth, Planetary, Space and Astronomical Research, Open University, Milton Keynes MK7 6AA, UK
Claire Cousins
Affiliation:
UK Centre for Astrobiology, School of Physics and Astronomy, University of Edinburgh, Edinburgh EH9 3JZ, UK
Paul T. Wilkinson
Affiliation:
Department of Physical Science, Centre for Earth, Planetary, Space and Astronomical Research, Open University, Milton Keynes MK7 6AA, UK
Karen Olsson-Francis
Affiliation:
Department of Physical Science, Centre for Earth, Planetary, Space and Astronomical Research, Open University, Milton Keynes MK7 6AA, UK
Ben Rozitis
Affiliation:
Department of Physical Science, Centre for Earth, Planetary, Space and Astronomical Research, Open University, Milton Keynes MK7 6AA, UK
*
e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The mean air temperature of the Icelandic interior is below 10 °C. However, we have previously observed 16S rDNA sequences associated with thermophilic lineages in Icelandic basalts. Measurements of the temperatures of igneous rocks in Iceland showed that solar insolation of these low albedo substrates achieved a peak surface temperature of 44.5 °C. We isolated seven thermophilic Geobacillus species from basalt with optimal growth temperatures of ~65 °C. The minimum growth temperature of these organisms was ~36 °C, suggesting that they could be active in the rock environment. Basalt dissolution rates at 40 °C were increased in the presence of one of the isolates compared to abiotic controls, showing its potential to be involved in active biogeochemistry at environmental temperatures. These data raise the possibility of transient active thermophilic growth in macroclimatically cold rocky environments, implying that the biogeographical distribution of active thermophiles might be greater than previously understood. These data show that temperatures measured or predicted over large scales on a planet are not in themselves adequate to assess niches available to extremophiles at micron scales.

Keywords

thermophilesextremophilesvolcanicMarsgeomicrobiology
Type
Research Article
Information
International Journal of Astrobiology , Volume 14 , Issue 3 , July 2015 , pp. 457 - 463
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnalds, O. (2004). Volcanic soils of Iceland. Catena 56, 3–20.Google Scholar
Banat, I.M., Marchant, R. & Rahman, T.J. (2004). Geobacillus debilis sp. nov., a novel obligately thermophilic bacterium isolated from a cool soil environment, and reassignment of Bacillus pallidus to Geobacillus pallidus comb. nov. Int. J. Syst. Evol. Microbiol. 54, 2197–2201.CrossRefGoogle Scholar
Barros, N., Feijóo, S., Salgado, J., Ramajo, B., Garcia, J.R. & Hansen, L.D. (2008). The dry limit of microbial life in the Atacama Desert revealed by calorimetric approaches. Eng. Life Sci. 8, 477–486.Google Scholar
Beaman, T.C., Pankratz, H.S. & Gerhardt, P. (1988). Heat shock affects permeability and resistance of Bacillus stearothermophilus spores. Appl. Environ. Microbiol. 54, 2515–2520.Google Scholar
Bruce, K.D., Hiorns, W.D., Hobman, J.L., Osborn, A.M., Strike, P. & Ritchie, D.A. (1992). Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl. Environ. Microbiol. 58, 3413–3416.CrossRefGoogle ScholarPubMed
Chen, C.-H., Wang, C.-H., Chen, D.-L., Sun, Y.-Y., Liu, J.-Y., Yeh, T.-K., Yen, H.-Y. & Chang, S.-H. (2011). Comparisons between air and subsurface temperatures in Taiwan for the past Century: a global warming perspective. In Groundwater and Subsurface Environments, ed. Taniguchi, M., pp. 185–199. Springer, Japan.Google Scholar
Claes, L. (1968). The minimum growth temperature of obligately thermophilic bacteria as influenced by inhibitors in complex growth media. Physiol. Plantarum 21, 26–34.Google Scholar
Cockell, C.S., Olsson, K., Knowles, F., Kelly, L., Herrera, A., Thorsteinsson, T. & Marteinsson, V. (2009). Bacteria in weathered basaltic glass, Iceland. Geomicrobiol. J. 26, 491–507.CrossRefGoogle Scholar
Cockell, C.S., Osinski, G.R. & Voytek, M.A. (2013). The geomicrobiology of impact structures. In Impact Cratering: Processes and Products, ed. Osinski, G.R. & Pierazzo, E., pp. 157–176. Wiley, Chichester.Google Scholar
Cousins, C.R. & Crawford, I.A. (2010). Volcano – Ice interaction as a microbial habitat on Earth and Mars. Astrobiology 11, 695–710.CrossRefGoogle Scholar
Crovisier, J.-L., Advocat, T. & Dussossoy, J.-L. (2003). Nature and role of natural alteration gels formed on the surface of ancient volcanic glasses (Natural analogs of waste containment glasses). J. Nucl. Mater. 321, 91–109.Google Scholar
de Rezende, J.R., Kjeldsen, K.U., Hubert, C.R., Finster, K., Loy, A. & Jørgensen, B.B. (2013) Dispersal of thermophilic Desulfotomaculum endospores into Baltic Sea sediments over thousands of years. ISME J. 7, 72–84.CrossRefGoogle ScholarPubMed
Dessert, C., Dupré, B., Gaillardet, J., François, L.M. & Allègre, C.J. (2003). Basalt weathering laws and the impact of basalt weathering on the global carbon cycle. Chem. Geol. 202, 257–273.CrossRefGoogle Scholar
Einarsson, M.Á., ed. (1984). Climate of Iceland. World Survey of Climatology: 15: Climates of the Oceans. Elsevier, Amsterdam.Google Scholar
Hall, K., Lindgren, B.S. & Jackson, P. (2005). Rock albedo and monitoring of thermal conditions in respect of weathering: some expected and some unexpected results. Earth Surface Process. Landforms 30, 801–811.Google Scholar
Herrera, A., Cockell, C.S., Self, S., Blaxter, M., Reitner, J., Gernot, A., Drose, W., Thorsteinsson, T. & Tindle, A.G. (2008). Bacterial colonization and weathering of terrestrial obsidian in Iceland. Geomicrobiol. J. 25, 25–37.Google Scholar
Herrera, A., Cockell, C.S., Self, S., Blaxter, M., Reitner, J., Thorsteinsson, T., Arp, G., Drose, W. & Tindle, A. (2009). A cryptoendolithic community in volcanic glass. Astrobiology 9, 369–381.CrossRefGoogle ScholarPubMed
Isaksen, M.F., Bak, F. & Jørgensen, B.B. (1994). Thermophilic sulfate-reducing bacteria in cold marine sediment. FEMS Microbiol. Ecol. 14, 1–8.Google Scholar
Kelly, L., Cockell, C.S., Piceno, Y.M., Andersen, G.L., Thorsteinsson, T. & Marteinsson, V. (2010). Bacterial diversity of weathered terrestrial Icelandic volcanic glasses. Microb. Ecol. 60, 740–752.Google Scholar
Kelly, L. et al. (2011). Bacterial diversity of terrestrial crystalline volcanic rocks, Iceland. Microb. Ecol. 62, 69–79.Google Scholar
Lawver, L.A. & Muller, R.D. (1994). Iceland hotspot track. Geology 22, 311–314.Google Scholar
Marchant, R., Banat, I.M., Rahman, T.J. & Berzano, M. (2002). The frequency and characteristics of highly thermophilic bacteria in cool soil environments. Environ. Microbiol. 4, 595–602.Google Scholar
Marchant, R., Franzetti, A., Pavlostathis, S.G., Tas, D.O., Erdbrugger, I., Unyayar, A., Mazmanci, M.A. & Banat, I.M. (2008). Thermophilic bacteria in cool temperate soils: are they metabolically active or continually added by global atmospheric transport? Appl. Microbiol. Biotechnol. 78, 841–852.Google Scholar
Markwell, M.K., Haas, S.M., Bieber, L.L. & Tolbert, N.E. (1979). A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87, 206–210.Google Scholar
McBean, G., Alekseev, G., Chen, D., Førland, E., Fyfe, J., Groisman, P.Y., King, , Melling, H., Vose, R. & Whitfield, P.H. (2005). Arctic Climate: Past and Present. Arctic Climate Impacts Assessment (ACIA). Cambridge University Press, Cambridge.Google Scholar
McGreevy, J.P. (1985). Thermal properties as controls on rock surface temperature maxima, and possible implications for rock weathering. Earth Surface Process. Landforms 10, 125–136.Google Scholar
McKay, C.P. & Friedmann, E.I. (1985). The cryptoendolithic microbial environment in the Antarctic cold desert: temperature variations in nature. Polar Biol. 4, 19–25.Google Scholar
Olsson-Francis, K., Simpson, A.E., Wolff-Boenisch, D. & Cockell, C.S. (2012). The effect of rock composition on cyanobacterial weathering of crystalline basalt and rhyolite. Geobiology 10, 434–444.Google Scholar
Pollack, H.N. & Huang, S. (2000). Climate reconstruction from subsurface temperatures. Annu. Rev. Earth Planet. Sci. 28, 339–365.Google Scholar
Robertson, E.C. & Peck, D.L. (1974) Thermal conductivity of vesicular basalt from Hawaii. J. Geophys. Res. 79, 4875–4888.Google Scholar
Schwieger, F. & Tebbe, C.C. (1998). A new approach to utilize PCR-single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl. Environ. Microbiol. 64, 4870–4876.Google Scholar
Striberger, J., Björck, S., Ingólfsson, O., Kjaer, K.H., Snowball, I. & Uvo, C.B. (2010). Climate variability and glacial processes in eastern Iceland during the past 700 years based on varved lake sediments. Boreas 40, 28–45.Google Scholar
Takacs-Vesbach, C., Mitchell, K., Jackson-Weaver, O. & Reysenbach, A.L. (2008). Volcanic calderas delineate biogeographical provinces among Yellowstone thermophiles. Environ. Microbiol. 10, 1681–1689.Google Scholar
Vary, J.C. & Halvorson, H.O. (1965) Kinetics of germination of Bacillus spores. J. Bacteriol. 89, 1340–1347.Google Scholar
Wu, L., Jacobson, A.D., Chen, H.-C. & Hausner, M. (2007) Characterisation of elemental release during microbe-basalt interactions at T = 28°C. Geochim. Cosmochim. Acta 71, 2224–2239.Google Scholar