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Open Research Online Oro.Open.Ac.Uk View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Open Research Online Open Research Online The Open University’s repository of research publications and other research outputs Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life Journal Item How to cite: Stevenson, Andrew; Burkhardt, Jürgen; Cockell, Charles S.; Cray, Jonathan A.; Dijksterhuis, Jan; Fox-Powell, Mark; Kee, Terence P.; Kminek, Gerhard; McGenity, Terry J.; Timmis, Kenneth N.; Timson, David J.; Voytek, Mary A.; Westall, Frances; Yakimov, Michail M. and Hallsworth, John E. (2015). Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environmental Microbiology, 17(2) pp. 257–277. For guidance on citations see FAQs. c 2014 Society for Applied Microbiology and John Wiley Sons Ltd Version: Version of Record Link(s) to article on publisher’s website: http://dx.doi.org/doi:10.1111/1462-2920.12598 Copyright and Moral Rights for the articles on this site are retained by the individual authors and/or other copyright owners. For more information on Open Research Online’s data policy on reuse of materials please consult the policies page. oro.open.ac.uk bs_bs_banner Environmental Microbiology (2015) 17(2), 257–277 doi:10.1111/1462-2920.12598 Minireview Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life Andrew Stevenson,1 Jürgen Burkhardt,2 Summary Charles S. Cockell,3 Jonathan A. Cray,1 Since a key requirement of known life forms is avail- Jan Dijksterhuis,4 Mark Fox-Powell,3 Terence P. Kee,5 able water (water activity; a ), recent searches for Gerhard Kminek,6 Terry J. McGenity,7 w signatures of past life in terrestrial and extraterrestrial Kenneth N. Timmis,8 David J. Timson,1 environments have targeted places known to have Mary A. Voytek,9 Frances Westall,10 contained significant quantities of biologically avail- Michail M. Yakimov11 and John E. Hallsworth1* able water. However, early life on Earth inhabited 1Institute for Global Food Security, School of Biological high-salt environments, suggesting an ability to with- Sciences, MBC, Queen’s University Belfast, Belfast, stand low water-activity. The lower limit of water activ- BT9 7BL, Northern Ireland. ity that enables cell division appears to be ∼ 0.605 2Plant Nutrition Group, Institute of Crop Science and which, until now, was only known to be exhibited by a Resource Conservation, University of Bonn, single eukaryote, the sugar-tolerant, fungal xerophile Karlrobert-Kreiten-Str. 13, D-53115 Bonn, Germany. Xeromyces bisporus. The first forms of life on Earth 3UK Centre for Astrobiology, School of Physics and were, though, prokaryotic. Recent evidence now indi- Astronomy, University of Edinburgh, Edinburgh EH9 cates that some halophilic Archaea and Bacteria have 3JZ, UK. water-activity limits more or less equal to those of 4CBS Fungal Biodiversity Centre, Uppsalalaan 8, CT X. bisporus. We discuss water activity in relation to 3584 Utrecht, The Netherlands. the limits of Earth’s present-day biosphere; the pos- 5School of Chemistry, University of Leeds, Leeds, LS2 sibility of microbial multiplication by utilizing water 9JT, West Yorkshire, UK. from thin, aqueous films or non-liquid sources; 6ESA-ESTEC, 2200 Noordwijk, The Netherlands. whether prokaryotes were the first organisms able to 7School of Biological Sciences, University of Essex, multiply close to the 0.605-a limit; and whether extra- Colchester, CO4 3SQ, Essex, UK. w terrestrial aqueous milieux of ≥ 0.605 a can resemble 8Institute of Microbiology, Technical University w fertile microbial habitats found on Earth. Braunschweig, Spielmannstrasse 7, D-38106 Braunschweig, Germany. 9NASA Headquarters, Washington, DC 20546-0001, Introduction USA. Given the fact that water is one of the principal ingredients 10 Centre de Biophysique Moléculaire, CNRS, Rue of cellular life (Daniel et al., 2004), insights into the Charles Sadron, Centre de Recherches sur les minimum water requirements of cells are imperative to Matériaux à Haute Température, 1D, avenue de la understanding both the functionality of living systems (at recherché scientifique, 45071 Orléans Cedex 2, France. every level, from biomacromolecule to biosphere) and the 11 CNR, Istituto per l’Ambiente Marino Costiero, 98122 origins of life itself. The generally held opinion is that life Messina, Italy. appeared independently on Earth and, possibly, else- where in the Solar System (Clancy et al., 2005), though one other explanation for the presence of life on Earth is that it appeared on another planet and was transported here in the form of prokaryotes or their ancestors (an idea known as panspermia; Thomson, 1871). Until recently, Received 3 June 2014; revised 8 August 2014; accepted 14 August 2014. *For correspondence. E-mail [email protected]; Tel. eukaryotic microbes have held the record for life under (+44) 289097 2314; Fax (+44) 289097 5877. water-constrained conditions, as some species are © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd 258 A. Stevenson et al. 1 capable of cell division down to a water activity (aw) of parameters are also used to designate the ‘special 0.605 at high sugar concentrations (Pitt and Christian, regions’ of Mars in which microbial cell division might 1968; Williams and Hallsworth, 2009). Whereas such data feasibly take place (Beaty et al., 2006; Kminek et al., have formed the basis for international policy for planetary 2010).3 The temperature window over which microbes protection in relation to space exploration missions (see are, collectively, capable of cell division (i.e. from −18°C below), sugar-rich substrates have very limited applicabil- to +122°C; Takai et al., 2008; Chin et al., 2010) spans ity to those extraterrestrial habitats with which we are ≤ 40% of the entire range of temperatures to which life familiar. Historically, the accepted limit for cell division of forms on Earth can be exposed (i.e. from approximately prokaryotic microbes has been 0.755 aw (for a small frac- −90°C to ≥ 250°C for some hydrothermal vents and the tion of halophilic species at high salt concentrations, see deep subsurface; Fig. 1A). By contrast, environmental Grant, 2004). However, both culture-based and culture- water-activity values range from 1 to ∼ 0, and the func- independent studies provide evidence for multiplication tional biosphere exists between 1 and ∼ 0.60 aw. Further- and metabolic activity of halophilic Archaea and Bacteria more, most cellular systems of known life forms on Earth down to 0.611 aw, both in their natural habitats in situ are only active within the range, or a segment of the and in vitro (Javor, 1984; Yakimov et al., 2014; A. Steven- range, 1 to 0.900 aw (Fig. 1B; Brown, 1976; Grant, 2004); son, J. A. Cray, J. P. Williams, R. Santos, R. Sahay, for example, there is a drop-off in the measurable activity N. Neuenkirchen, C. D. McClure, I. R. Grant, J. D. R. of soil microbiota at < 0.890 aw (Manzoni et al., 2012; Houghton, J. P. Quinn, D. J., Timson, S. V. Patil, R. S. Moyano et al., 2013; Stevenson and Hallsworth, 2014). Singhal, J. B. Antón, J. Dijksterhuis, A. D. Hocking, However, metabolic activity and cell division has B. Lievens, D. E. N. Rangel, M. A. Voytek, N. Gunde- been reported below 0.900 aw for a great number Cimerman, A. Oren, K. N. Timmis, T. J. McGenity, and J. of xerotolerant/philic and halotolerant/philic microbes 2 E. Hallsworth, submitted). Whereas the vast majority of (Brown, 1976; Grant, 2004), and even below 0.755 aw for yeasts and fungi are active somewhere within the range 1 both eukaryotic and prokaryotic species (Javor, 1984; to 0.900 aw (or within a segment of this range; for exam- Williams and Hallsworth, 2009; Yakimov et al., 2014; A. ples, see Brown, 1976; Hallsworth and Magan, 1994; Stevenson, J. A. Cray, J. P. Williams, R. Santos, R. Kashangura et al., 2006), only ∼12 species have been Sahay, N. Neuenkirchen, C. D. McClure, I. R. Grant, observed to grow and/or germinate at < 0.700 aw J. D. R. Houghton, J. P. Quinn, D. J., Timson, S. V. Patil, (Williams and Hallsworth, 2009; A. Stevenson, J. A. Cray, R. S. Singhal, J. B. Antón, J. Dijksterhuis, A. D. Hocking, J. P. Williams, R. Santos, R. Sahay, N. Neuenkirchen, C. B. Lievens, D. E. N. Rangel, M. A. Voytek, N. Gunde- D. McClure, I. R. Grant, J. D. R. Houghton, J. P. Quinn, D. Cimerman, A. Oren, K. N. Timmis, T. J. McGenity, and J., Timson, S. V. Patil, R. S. Singhal, J. B. Antón, J. J. E. Hallsworth, submitted). Of the microbes known to Dijksterhuis, A. D. Hocking, B. Lievens, D. E. N. Rangel, multiply below 0.720, the majority (unlike Xeromyces M. A. Voytek, N. Gunde-Cimerman, A. Oren, K. N. Timmis, bisporus) are not obligate osmophiles that are only T. J. McGenity, and J. E. Hallsworth, submitted). Here, we discuss the evidence for microbial activity in habitats at or 3See also J. D. Rummel, D. W. Beaty, M. A. Jones, C. Bakermans, N. below 0.690 aw which represent the very fringe of the G. Barlow, P. Boston, V. Chevrier, B. Clark, J.-P. de Vera, R. V. Gough, functional biosphere on Earth. Low water-activity environ- J. E. Hallsworth, J. W. Head, V. J. Hipkin, T. L. Kieft, A. S. McEwen, M. T. Mellon, J. Mikucki, W. L. Nicholson, C. R. Omelon, R. Peterson, ments are also discussed in relation to early life on Earth, E. Roden, B. Sherwood Lollar, K. L. Tanaka, D. Viola and J. J. Wray, the plausibility of cell division in extraterrestrial environ- unpublished. Planetary-protection policy, in relation to space mis- ments which contain biologically available water and a sions, aims to protect those planets where spacecraft are landed, as well as Earth, from accidental contamination with non-native life forms series of unanswered scientific questions.
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