Limits of life in hostile environments: no barriers to biosphere function?

Abstract

SummaryEnvironments that are hostile to life are characterized by reduced microbial activity which results in poor soil-and plant-health, low biomass and biodiversity, and feeble ecosystem development. Whereas the functional biosphere may primarily be constrained by water activity (a w) the mechanism(s) by which this occurs have not been fully elucidated. Remarkably we found that, for diverse species of xerophilic fungi at a w values of Յ 0.72, water activity per se did not limit cellular function. We provide evidence that chaotropic activity determined their biotic window, and obtained mycelial growth at water activities as low as 0.647 (below that recorded for any microbial species) by addition of compounds that reduced the net chaotropicity. Unexpectedly we found that some fungi grew optimally under chaotropic conditions, providing evidence for a previously uncharacterized class of extremophilic microbes. Further studies to elucidate the way in which solute activities interact to determine the limits of life may lead to enhanced biotechnological processes, and increased productivity of agricultural and natural ecosystems in arid and semiarid regions.

Solutes determine the temperature windows for microbial survival and growth

“…In accordance with our hypothesis (but nevertheless, to our surprise), cells preferentially synthesized and accumulated a chaotropic-compatible solute, glycerol ( Fig. 3B) (13). It is energy expensive to both synthesize compatible solutes de novo and to retain them in the cell, and indeed, the cost imposed to the cellular system is known to determine the limits of microbial growth windows under stressful conditions (e.g., low water activity or ethanol stress) (21,22).…”

“…2 R-T). Although the mechanisms by which diverse solutes exert chaotropic activity are not yet wellunderstood, the net effects of ionic, nonionic, and hydrophobic chaotropes (9, 10, 18) may be indistinguishable to the cell (13). † Our data show that M. frigida growth was rapid at the highest incubation temperature (+1.7°C), regardless of medium type, but that growth rates were greatly enhanced on all chaotropesupplemented media relative to that on the kosmotropic medium at subzero temperatures ( Fig.…”

“…Generally low temperatures promote noncovalent interactions and, thereby, rigidify cellular macromolecules and membranes (2). Conversely, chaotropic solutes are known to disorder macromolecular systems, inducing a potent form of cellular stress (10), and they are known to limit the functional biosphere in some locations on Earth (11)(12)(13). * We formulated the hypothesis that chaotropic substances which under many circumstances act as stressors can, nevertheless, enhance cellular activity at suboptimal growth temperatures and thereby extend the biotic windows of microbial cells in cold environments.…”

Metagenomic analysis of the bacterial microbiota linked to the traditional Algerian date product “Btana”

“…Grant (2004) revealed that high-sugar foods (with low aw) are mainly dominated by xerophilic fungi and osmophilic yeasts. However, the presence of halotolerant bacteria in these foods was often reported, although the osmotic stress imposed by cations (salts) and uncharged organic solutes (like sucrose) is not the same (Williams and Hallsworth 2009). Recently, a halotolerant bacterium Tetragenococcus halophilus was found to be dominant (>99 %) in a high-sugar Bthick juice^ (Justé et al 2008).…”

“…Thus, it is expected that one would find many halotolerant bacteria in Btana samples, such as: Corynebacterium, Acinetobacter, Acidovorax, Propionibacterium, Staphylococcus and Peptostreptococcus (De Vos et al 2009). Moreover, osmotolerance is linked with the availability of osmoprotectants in the surrounding medium to help bacteria to maintain the internal homeostasis (Williams and Hallsworth 2009). Interestingly, it was reported that dates are very rich in proline (12-369 mg/100 g), choline (6.30-9.90 mg/100 g), betaine (0.4 mg/100 g), and also contain a high level of potassium (703-1130 mg/100 g) (Favier et al 1993;Al-Shahib and Marshall 2002;El-Sohaimy and Hafez 2010;Kchaou et al 2013).…”