Solutes determine the temperature windows for microbial survival and growth

Abstract

Microbial cells, and ultimately the Earth's biosphere, function within a narrow range of physicochemical conditions. For the majority of ecosystems, productivity is cold-limited, and it is microbes that represent the failure point. This study was carried out to determine if naturally occurring solutes can extend the temperature windows for activity of microorganisms. We found that substances known to disorder cellular macromolecules (chaotropes) did expand microbial growth windows, fungi preferentially accumulated chaotropic metabolites at low temperature, and chemical activities of solutes determined microbial survival at extremes of temperature as well as pressure. This information can enhance the precision of models used to predict if extraterrestrial and other hostile environments are able to support life; furthermore, chaotropes may be used to extend the growth windows for key microbes, such as saprotrophs, in cold ecosystems and manmade biomes.

Reduction of the Temperature Sensitivity of Halomonas hydrothermalis by Iron Starvation Combined with Microaerobic Conditions

“…The sea ice bacterium Shewanella gelidimarina, for example, has been shown to exhibit an increased temperature range for cell division when cultured at high (NaCl) salinity, with increases in membrane lipid packing and fatty acid content conferring tolerance of both conditions (13). Other solutes (including MgCl 2 ) have also been found to influence the temperature limits for microbial multiplication (15,17). Moreover, adaptation to high hydrostatic pressure has been proposed as a mechanism that enables bacterial multiplication within hypersaline deep-sea environments (14).…”

“…Despite our knowledge of the physicochemical boundaries for microbial cell division having been greatly advanced over the past three decades, we are only beginning to understand how interactions between different stressors define biological permissiveness for natural ecosystems (8,(13)(14)(15)(16)(17)(18). In particular, while several studies have identified minimal and maximal limits for microbial life in response to the surrounding environment (1,5,(19)(20)(21), there is a paucity of information on how rates of cell division are impacted by multiple stress parameters within extreme habitats.…”

“…An increasing body of evidence suggests that it is frequently the net effect of diverse stress parameters that defines the boundary space for life (8,(13)(14)(15)(16)(17)(18). The sea ice bacterium Shewanella gelidimarina, for example, has been shown to exhibit an increased temperature range for cell division when cultured at high (NaCl) salinity, with increases in membrane lipid packing and fatty acid content conferring tolerance of both conditions (13).…”

Biosynthesis of the Osmoprotectant Ectoine, but Not Glycine Betaine, Is Critical for Survival of Osmotically Stressed Vibrio parahaemolyticus Cells

“…We showed using one-dimension 1 H nuclear magnetic resonance spectroscopy ( 1 H-NMR) that at high salinity V. parahaemolyticus is capable of de novo synthesis of ectoine whereas a ⌬ectB strain is not (25). In a broader context, it has been shown that compatible solutes and solute activities can protect against nonosmotic stresses, for example high-pressure stress can be countered by kosmotropes (36), while some studies have shown that compatible solutes can crossprotect against heat and cold-temperature stress (27,37,38).…”

Modulating Nucleation by Kosmotropes and Chaotropes: Testing the Waters

“…In view of the pre-nucleation regime, opposite outcomes are elicited by chaotropes. This is evident from the decreased slope of the pre-nucleation regimes corresponding to 30,22, and 14% in presence of urea, guanidium and thiourea, respectively at pH 9.75. These effects are diminished at pH 9.0, however, urea retains its effect as a PNC stabilizer at pH 9.0 and 9.75.…”