Limits of life in MgCl₂‐containing environments: chaotropicity defines the window

Abstract

The biosphere of planet Earth is delineated by physico-chemical conditions that are too harsh for, or inconsistent with, life processes and maintenance of the structure and function of biomolecules. To define the window of life on Earth (and perhaps gain insights into the limits that life could tolerate elsewhere), and hence understand some of the most unusual biological activities that operate at such extremes, it is necessary to understand the causes and cellular basis of systems failure beyond these windows. Because water plays such a central role in biomolecules and bioprocesses, its availability, properties and behaviour are among the key life-limiting parameters. Saline waters dominate the Earth, with the oceans holding 96.5% of the planet's water. Saline groundwater, inland seas or saltwater lakes hold another 1%, a quantity that exceeds the world's available freshwater. About one quarter of Earth's land mass is underlain by salt, often more than 100 m thick. Evaporite deposits contain hypersaline waters within and between their salt crystals, and even contain large subterranean salt lakes, and therefore represent significant microbial habitats. Salts have a major impact on the nature and extent of the biosphere, because solutes radically influence water's availability (water activity) and exert other activities that also affect biological systems (e.g. ionic, kosmotropic, chaotropic and those that affect cell turgor), and as a consequence can be major stressors of cellular systems. Despite the stressor effects of salts, hypersaline environments can be heavily populated with salt-tolerant or -dependent microbes, the halophiles. The most common salt in hypersaline environments is NaCl, but many evaporite deposits and brines are also rich in other salts, including MgCl 2 (several hundred million tonnes of bischofite, MgCl2·6H2O, occur in one formation alone). Magnesium (Mg) is the third most abundant element dissolved in seawater and is ubiquitous in the Earth's crust, and throughout the Solar System, where it exists in association with a variety of anions. Magnesium chloride is exceptionally soluble in water, so can achieve high concentrations (> 5 M) in brines. However, while NaCldominated hypersaline environments are habitats for a rich variety of salt-adapted microbes, there are contradictory indications of life in MgCl 2-rich environments. In this work, we have sought to obtain new insights into how MgCl2 affects cellular systems, to assess whether MgCl2 can determine the window of life, and, if so, to derive a value for this window. We have dissected two relevant cellular stress-related activities of MgCl2 solutions, namely water activity reduction and chaotropicity, and analysed signatures of life at different concentrations of MgCl2 in a natural environment, namely the 0.05-5.05 M MgCl2 gradient of the seawater : hypersaline brine interface of Discovery Basin -a large, stable brine lake almost saturated with MgCl2, located on the Mediterranean Sea floor. We document here the exceptional chaotropicity...

Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea

“…The interface was captured and fractionated as described previously (Daffonchio et al, 2006;Hallsworth et al, 2007). Briefly, 10-litre Niskin bottles housed on a rosette with conductivity-temperature-depth sensors were closed when a large increase in conductivity, indicating that the interface had been entered, was observed.…”

“…Sulfide concentrations were measured photometrically by the methylene blue method (Cline, 1969). Redox potentials (Eh) of unfiltered sample aliquots were measured immediately according to the procedure described by Daffonchio et al (2006) and Hallsworth et al (2007). Major elements including nitrate and ammonia were analyzed by Stayer 1C isocratic chromatography system for routine ion determination (Portlab, Sulmona, Italy).…”

“…Sequence analysis was performed as described previously (Hallsworth et al, 2007;Yakimov et al, 2007). Briefly, all sequences were edited with MacVector Software version 7.2.2 (Accelrys, San Diego, CA, USA) and compared with DNA or aminoacid sequences in the public domain through the Basic Local Alignment Search Tool (BLAST) (Altschul et al, 1997).…”

“…They were formed 5000-40 000 years ago by dissolution of ancient subterranean salt deposits (Messinian evaporites) exposed to seawater by tectonic shifts and the downward flow of the dense brines into local abyssal depressions, followed by progressive development of anoxia in the brine lakes thereby formed (Fusi et al, 1996;Wallmann et al, 1997). Recent studies of DHALs revealed the existence of new microbial lineages flourishing within these harsh environments (Ferrer et al, 2005;van der Wielen et al, 2005;Daffonchio et al, 2006;Hallsworth et al, 2007;Yakimov et al, 2007).…”

Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin

“…Thus far, DHABs in the Mediterranean and Red Sea have provided exciting new insights into novel microbial diversity and have extended our knowledge of environmental factors that define the limits of life (Eder et al, 1999(Eder et al, , 2001Hallsworth et al, 2007). Studies of Discovery, L'Atalante, Urania, Thetis and Bannock basins revealed that DHAB interfaces harbor abundant and diverse microbial communities that include numerous novel candidate divisions that are more productive than most pelagic marine systems (see, for example, Sass et al, 2001;Van Der Wielen et al, 2005;Yakimov et al, 2007;Edgcomb et al, 2009;Stock et al, 2012).…”