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Concomitant osmotic and chaotropicity-induced stresses in Aspergillus wentii: compatible solutes determine the biotic window

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Abstract

Whereas osmotic stress response induced by solutes has been well-characterized in fungi, less is known about the other activities of environmentally ubiquitous substances. The latest methodologies to define, identify and quantify chaotropicity, i.e. substance-induced destabilization of macromolecular systems, now enable new insights into microbial stress biology (Cray et al. in Curr Opin Biotechnol 33:228–259, 2015a, doi:10.1016/j.copbio.2015.02.010; Ball and Hallsworth in Phys Chem Chem Phys 17:8297–8305, 2015, doi:10.1039/C4CP04564E; Cray et al. in Environ Microbiol 15:287–296, 2013a, doi:10.1111/1462-2920.12018). We used Aspergillus wentii, a paradigm for extreme solute-tolerant fungal xerophiles, alongside yeast cell and enzyme models (Saccharomyces cerevisiae and glucose-6-phosphate dehydrogenase) and an agar-gelation assay, to determine growth-rate inhibition, intracellular compatible solutes, cell turgor, inhibition of enzyme activity, substrate water activity, and stressor chaotropicity for 12 chemically diverse solutes. These stressors were found to be: (i) osmotically active (and typically macromolecule-stabilizing kosmotropes), including NaCl and sorbitol; (ii) weakly to moderately chaotropic and non-osmotic, these were ethanol, urea, ethylene glycol; (iii) highly chaotropic and osmotically active, i.e. NH4NO3, MgCl2, guanidine hydrochloride, and CaCl2; or (iv) inhibitory due primarily to low water activity, i.e. glycerol. At ≤0.974 water activity, Aspergillus cultured on osmotically active stressors accumulated low-M r polyols to ≥100 mg g dry weight−1. Lower-M r polyols (i.e. glycerol, erythritol and arabitol) were shown to be more effective for osmotic adjustment; for higher-M r polyols such as mannitol, and the disaccharide trehalose, water-activity values for saturated solutions are too high to be effective; i.e. 0.978 and 0.970 (25 ºC). The highly chaotropic, osmotically active substances exhibited a stressful level of chaotropicity at physiologically relevant concentrations (20.0–85.7 kJ kg−1). We hypothesized that the kosmotropicity of compatible solutes can neutralize chaotropicity, and tested this via in-vitro agar-gelation assays for the model chaotropes urea, NH4NO3, phenol and MgCl2. Of the kosmotropic compatible solutes, the most-effective protectants were trimethylamine oxide and betaine; but proline, dimethyl sulfoxide, sorbitol, and trehalose were also effective, depending on the chaotrope. Glycerol, by contrast (a chaotropic compatible solute used as a negative control) was relatively ineffective. The kosmotropic activity of compatible solutes is discussed as one mechanism by which these substances can mitigate the activities of chaotropic stressors in vivo. Collectively, these data demonstrate that some substances concomitantly induce chaotropicity-mediated and osmotic stresses, and that compatible solutes ultimately define the biotic window for fungal growth and metabolism. The findings have implications for the validity of ecophysiological classifications such as ‘halophile’ and ‘polyextremophile’; potential contamination of life-support systems used for space exploration; and control of mycotoxigenic fungi in the food-supply chain.

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Acknowledgments

The authors wish to thank Philip Ball for scientifically stimulating discussions. Funding was supplied by the University of Stellenbosch (South Africa) and EU grants MIFRIEND and BIODEEP who supported JE Hallsworth and FL Alves; the Department of Agriculture and Rural Development (Northern Ireland) who supported A Stevenson; and grants from the São Paulo Research Foundation (FAPESP) of Brazil (#2010/06374-1, #2013/50518-6 and #2014/01229-4) and the Brazilian National Council for Scientific and Technological Development (CNPq) (#PQ2 302312/2011-0 and #PQ1D 308436/2014-8) which supported DEN Rangel.

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Author notes

  1. Ian E. G. Morrison

    Present address: Department of Biology, University of York, Heslington, York, YO10 5DD, UK

  2. Kenneth N. Timmis

    Present address: Institute of Microbiology, Technical University Braunschweig, Spielmannstrasse 7, 38106, Brunswick, Germany

Authors and Affiliations

  1. Department of Biological Sciences, University of Essex, Colchester, CO4 3SQ, UK

    Flávia de Lima Alves, Jenny L. M. Gillion, Fakhrossadat Hejazi, Sandra Hayes, Ian E. G. Morrison, Terry J. McGenity, Kenneth N. Timmis & John E. Hallsworth

  2. Institute of Global Food Security, School of Biological Sciences, MBC, Queen’s University Belfast, Belfast, BT9 7BL, Northern Ireland, UK

    Andrew Stevenson & John E. Hallsworth

  3. Applied Mycology Group, Cranfield Soil and AgriFood Institute, Cranfield University, Cranfield, Bedford, MK43 OAL, UK

    Esther Baxter & Naresh Magan

  4. Department of Microbiology, University of Stellenbosch, Matieland, 7602, South Africa

    Bernard A. Prior & John E. Hallsworth

  5. Instituto de Pesquisa e Desenvolvimento, Universidade do Vale do Paraíba, São José dos Campos, SP, 12244-000, Brazil

    Drauzio E. N. Rangel

Authors
  1. Flávia de Lima Alves
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  2. Andrew Stevenson
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  6. Sandra Hayes
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  7. Ian E. G. Morrison
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  10. Drauzio E. N. Rangel
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  11. Naresh Magan
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  13. John E. Hallsworth
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Corresponding author

Correspondence to John E. Hallsworth.

Additional information

Communicated by D. E. N. Rangel.

This article is part of the Special Issue “Fungal Stress Responses”.

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de Lima Alves, F., Stevenson, A., Baxter, E. et al. Concomitant osmotic and chaotropicity-induced stresses in Aspergillus wentii: compatible solutes determine the biotic window. Curr Genet 61, 457–477 (2015). https://doi.org/10.1007/s00294-015-0496-8

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