Water-, pH- and temperature relations of germination for the extreme xerophiles Xeromyces bisporus (FRR 0025), Aspergillus penicillioides (JH06THJ) and Eurotium halophilicum (FRR 2471).

Andrew Stevenson,John E Hallsworth,Jan Dijksterhuis,Philip G Hamill

doi:10.1111/1751-7915.12406

Andrew Stevenson, John E Hallsworth + Show 2 more

Open Access

https://doi.org/10.1111/1751-7915.12406

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Abstract

SummaryWater activity, temperature and pH are determinants for biotic activity of cellular systems, biosphere function and, indeed, for all life processes. This study was carried out at high concentrations of glycerol, which concurrently reduces water activity and acts as a stress protectant, to characterize the biophysical capabilities of the most extremely xerophilic organisms known. These were the fungal xerophiles: Xeromyces bisporus (FRR 0025), Aspergillus penicillioides (JH06THJ) and Eurotium halophilicum (FRR 2471). High‐glycerol spores were produced and germination was determined using 38 media in the 0.995–0.637 water activity range, 33 media in the 2.80–9.80 pH range and 10 incubation temperatures, from 2 to 50°C. Water activity was modified by supplementing media with glycerol+sucrose, glycerol+NaCl and glycerol+NaCl+sucrose which are known to be biologically permissive for X. bisporus, A. penicillioides and E. halophilicum respectively. The windows and rates for spore germination were quantified for water activity, pH and temperature; symmetry/asymmetry of the germination profiles were then determined in relation to supra‐ and sub‐optimal conditions; and pH‐ and temperature optima for extreme xerophilicity were quantified. The windows for spore germination were ~1 to 0.637 water activity, pH 2.80–9.80 and > 10 and < 44°C, depending on strain. Germination profiles in relation to water activity and temperature were asymmetrical because conditions known to entropically disorder cellular macromolecules, i.e. supra‐optimal water activity and high temperatures, were severely inhibitory. Implications of these processes were considered in relation to the in‐situ ecology of extreme conditions and environments; the study also raises a number of unanswered questions which suggest the need for new lines of experimentation.

Highlights

Xerophilic fungi act as pioneers under hostile conditions, and can catalyse ecosystem development at low water-availability
Water activity was modified by supplementing media with glycerol+sucrose, glycerol+NaCl and glycerol+NaCl+sucrose which are known to be biologically permissive for X. bisporus, A. penicillioides and E. halophilicum respectively
Understanding xerophile behaviour in relation to environmental constraints facilitates our understanding of the biophysical limits for life and addresses important questions relating to the issue of habitability of hostile environments, including those which lie at the heart of the astrobiology field (Rummel et al, 2014)

Summary

Temperature optima for extreme xerophilicity were quantified. The windows for spore germination were ~1 to 0.637 water activity, pH 2.80–9.80 and > 10 and < 44°C, depending on strain. Germination profiles in relation to water activity and temperature were asymmetrical because conditions known to entropically disorder cellular macromolecules, i.e. supra-optimal water activity and high temperatures, were severely inhibitory. Implications of these processes were considered in relation to the in-situ ecology of extreme conditions and environments; the study raises a number of unanswered questions which suggest the need for new lines of experimentation

Introduction

Results and discussion

Concluding remarks

Experimental procedures