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Environmental Microbiology (2015) 17(2), 255–256

doi:10.1111/1462-2920.12694

Highlight Salty worlds underwater

Josefa Antón* Department of Physiology, Genetics, and Microbiology, University of Alicante, Alicante 03080, Spain.

Yakimov and colleagues (2015) present in this issue of Environmental Microbiology the analysis of life under one of the most extreme environments on Earth: a submarine anoxic hypersaline lake, located in the Eastern Mediterranean basin. This work opens up fascinating questions regarding the geochemical windows for microbial extremophiles, the evolution and dispersal of communities in such physically isolated environments, and the metabolisms and stress tolerance mechanisms of their inhabitants. However, the interest of this work goes beyond microbial ecology and will likely have an impact on the search for extra-terrestrial life. Deep down, thousands of metres below sea level, the Mediterranean Sea harbours hypersaline lakes derived from the dissolution of evaporites formed during the Messinian salinity crisis. Geologists use that name to refer to the desiccation events that took place in the Mediterranean about 6 million years ago which resulted in a massive precipitation of sea salts that gave rise to evaporitic rocks of different compositions (De Lange et al., 2008). Due to several geological processes in the Mediterranean Ridge, some of these Messinian evaporites ended up dissolved in submarine brine lakes within confined depressions. These extreme systems, known as ‘deep hypersaline anoxic lakes’ (DHALs), have salt concentrations 5–10 times higher than seawater, lack oxygen and light, and are exposed to high pressure. Given their high density, DHALs are separated from the overlaying seawater by a thin and normally very stable chemo/redox/pycnocline characterized by a stratified succession of different electron donors and acceptors that can support a diverse microbial community. These transition zones are normally enriched in comparison to overlying seawater and underlying brines (Mapelli et al., 2012). In fact, some DHALS and their overlying seawater

*For correspondence. E-mail [email protected]; Tel. 34 965903870; Fax 34 965909569.

© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd

can be populated by a diverse community of extremely halophilic microbes, including lineages that were originally discovered in these systems, which so far remain uncultured. This is the case for instance of the euryarchaea MSBL-1 (a putative group of methanogens) or the bacteria KB-1, which have been shown to establish trophic cooperation (Yakimov et al., 2013). Since the 1980s (De Lange and Ten Haven, 1983), a total of eight DHALs have been discovered on the Mediterranean floor (Fig. 1), although microbiology studies started only a decade ago (Van der Wielen et al., 2005). These DHALs differ in their salt composition and, accordingly, in their microbial communities. It was the study of one such system, the Discovery basin, that set the limits of life in MgCl2-containing environments. In a seminal paper, Hallsworth and colleagues (2007) showed that it is MgCl2 and not salt concentration per se that restricts life in many hypersaline environments. This is due to the effects that different salts can have on cells. Although all solutes reduce water availability (i.e. water activity), some, like MgCl2, can act as chaotropes, weakening electrostatic interactions and hence destabilizing biological molecules. Others, like NaCl, are kosmotropes that strengthen these interactions and stabilize macromolecules. By monitoring signatures of life at the 0.05–5.05 M MgCl2 seawater : brine interface of the Discovery basin, the authors showed that chaotropicity, rather than water activity reduction, inhibited life by denaturing biological molecules. These authors stated that, in the absence of kosmotropes, the upper MgCl2 concentration for life is about 2.3 M, although they left the door open to the existence of life at higher concentrations in the presence of stabilizing solutes. In this issue, a team including many of the authors of Hallsworth and colleagues (2007) shows that indeed life can exist above the MgCl2 limit provided that other kosmotropic salts compensate for its chaotropic effects (Yakimov et al., 2015). These authors describe the exciting discovery of Lake Kryos, a new DHAL, so far the largest athalassohaline formation on Earth, with a salinity of 47% and around 4.3 M MgCl2. Together with the Discovery basin and the Antarctic Don Juan pond, these are the three saltiest aquatic habitats described so far on our planet. Lake Kryos has a composition similar to the

256 J. Antón

Fig. 1. Location of the eight currently known DHALs in the Eastern Mediterranean. Adapted from Yakimov and colleagues (2015).

Discovery basin but with higher Na+ and SO42− concentrations and thus it is an excellent scenario to explore the compensating effects of kosmotropic solutes. The authors were able to recover mRNA from the 2.27–3.03 M MgCl2 layer of the seawater : brine interface (equivalent to 0.747–0.631 water-activity) thereby expanding the established chaotropicity window for life that was set at 0.790 water activity. Again among the likely inhabitants were KB1 and MSBL1, for which close relatives have been detected in sediments from solar lakes and salterns. Together with the significance of this study in the fields of microbial ecology and evolution, its findings have clear implications in the search for extra-terrestrial life, since Mg is present in high concentrations on Mars and possibly Jupiter’s moon Europa. Once again, the outcomes of environmental microbiology studies surpass the physical limits of the system under study. It seems that Simon Conway Morris (2010) was right when he pointed out that ‘if you want to understand aliens, stay at home’. References Conway Morris, S. (2010) Aliens at home? EMBO Rep 11: 563. De Lange, G., Van Santvoort, P.J.M., Brumsack, H.J., Dählmann, A., and Reitz, A. (2008) A preliminary assessment of the composition of evaporites underlying the

Eastern Mediterranean seafloor using pore water. In The Messinian Salinity Crisis from mega-deposits to microbiology-A consensus report. N° 33 in CIESM Workshop Monographs. F. Briand (ed.) Monaco: CIESM, pp. 111–115. De Lange, G.J., and Ten Haven, H.L. (1983) Recent sapropel formation in the Eastern Mediterranean. Nature 305: 797– 798. Hallsworth, J.E., Yakimov, M.M., Golyshin, P.N., Gillion, J.L., D’Auria, G., de Lima Alves, F., et al. (2007) Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ Microbiol 9: 801–813. Mapelli, F., Borin, S., and Daffonchio, D. (2012) Microbial diversity in deep hypersaline anoxic basins. In Adaption of Microbial Life to Environmental Extremes. Stan-Lotterand, H., and Fendrihan, S. (eds). Wien, Austria: SpringerVerlag, pp. 21–36. Van der Wielen, P.J.J.J., Bolhuis, H., Borin, S., Daffonchio, D., Corselli, C., Giuliano, L., et al. (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307: 121–123. Yakimov, M.M., La Cono, V., Slepak, V.Z., La Spada, G., Arcadi, E., Messina, E., et al. (2013) Microbial life in the Lake Medee, the largest deep-sea salt-saturated formation. Sci Rep 3: 3554. doi:10.1038/srep03554. Yakimov, M.M., La Cono, V., La Spada, G., Bortoluzzi, G., Messina, E., Smedile, F., et al. (2015) Microbial community of the deep-sea brine Lake Kryos seawater-brine interface is active below the chaotropicity limit of life as revealed by recovery of mRNA. Environ Microbiol.

© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology, 17, 255–256

Salty worlds underwater.

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