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Stress Adaptation

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  • Authors: Alistair J. P. Brown1, Leah E. Cowen2, Antonio di Pietro3, Janet Quinn4
  • Editors: Joseph Heitman5, Neil A. R. Gow6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Medical Research Council Centre for Medical Mycology at the University of Aberdeen, Aberdeen Fungal Group, University of Aberdeen, Institute of Medical Sciences, Foresterhill, Aberdeen AB25 2ZD, United Kingdom; 2: Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada M5S 1A8; 3: Departamento de Genética, Universidad de Córdoba, Campus de Rabanales, Edificio Gregor Mendel C5, 14071 Córdoba, Spain; 4: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, United Kingdom; 5: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 6: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
  • Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0048-2016
  • Received 06 March 2017 Accepted 11 May 2017 Published 14 July 2017
  • Alistair J. P. Brown, al.brown@abdn.ac.uk
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  • Abstract:

    Fungal species display an extraordinarily diverse range of lifestyles. Nevertheless, the survival of each species depends on its ability to sense and respond to changes in its natural environment. Environmental changes such as fluctuations in temperature, water balance or pH, or exposure to chemical insults such as reactive oxygen and nitrogen species exert stresses that perturb cellular homeostasis and cause molecular damage to the fungal cell. Consequently, fungi have evolved mechanisms to repair this damage, detoxify chemical insults, and restore cellular homeostasis. Most stresses are fundamental in nature, and consequently, there has been significant evolutionary conservation in the nature of the resultant responses across the fungal kingdom and beyond. For example, heat shock generally induces the synthesis of chaperones that promote protein refolding, antioxidants are generally synthesized in response to an oxidative stress, and osmolyte levels are generally increased following a hyperosmotic shock. In this article we summarize the current understanding of these and other stress responses as well as the signaling pathways that regulate them in the fungi. Model yeasts such as are compared with filamentous fungi, as well as with pathogens of plants and humans. We also discuss current challenges associated with defining the dynamics of stress responses and with the elaboration of fungal stress adaptation under conditions that reflect natural environments in which fungal cells may be exposed to different types of stresses, either sequentially or simultaneously.

  • Citation: Brown A, Cowen L, di Pietro A, Quinn J. 2017. Stress Adaptation. Microbiol Spectrum 5(4):FUNK-0048-2016. doi:10.1128/microbiolspec.FUNK-0048-2016.

Key Concept Ranking

RNA Polymerase II
0.5083333
Programmed Cell Death
0.486292
Human Pathogenic Fungi
0.4425484
Cellular Processes
0.43688503
0.5083333

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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0048-2016
2017-07-14
2017-07-25

Abstract:

Fungal species display an extraordinarily diverse range of lifestyles. Nevertheless, the survival of each species depends on its ability to sense and respond to changes in its natural environment. Environmental changes such as fluctuations in temperature, water balance or pH, or exposure to chemical insults such as reactive oxygen and nitrogen species exert stresses that perturb cellular homeostasis and cause molecular damage to the fungal cell. Consequently, fungi have evolved mechanisms to repair this damage, detoxify chemical insults, and restore cellular homeostasis. Most stresses are fundamental in nature, and consequently, there has been significant evolutionary conservation in the nature of the resultant responses across the fungal kingdom and beyond. For example, heat shock generally induces the synthesis of chaperones that promote protein refolding, antioxidants are generally synthesized in response to an oxidative stress, and osmolyte levels are generally increased following a hyperosmotic shock. In this article we summarize the current understanding of these and other stress responses as well as the signaling pathways that regulate them in the fungi. Model yeasts such as are compared with filamentous fungi, as well as with pathogens of plants and humans. We also discuss current challenges associated with defining the dynamics of stress responses and with the elaboration of fungal stress adaptation under conditions that reflect natural environments in which fungal cells may be exposed to different types of stresses, either sequentially or simultaneously.

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Image of FIGURE 1
FIGURE 1

Cartoon summarizing stress pathways in the model fungus . See text. This figure summarizes some, but not all, of the known components of these signaling pathways. Components of MAPK signaling modules are highlighted in blue, transcription factors in pink, components of the calmodulin-calcineurin pathway in cyan, Rim pathway components in green, and the molecular chaperone Hsp90 in yellow. Note that the Cek1 MAPK pathway, which contributes to cell wall remodeling in this fungus, is included (dark blue ovals with white lettering).

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0048-2016
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Image of FIGURE 2
FIGURE 2

The CSR can lead to stress cross-protection. CSRs, which have been defined by genome-wide transcriptional profiling, represent the set of genes that is commonly up- or downregulated by different types of stress (see text). This Venn diagram illustrates the conceptual overlap between these sets of genes, highlighting the core stress genes. A CSR can lead to stress cross-protection during exposure to sequential stresses; i.e., cells that are exposed to one type of stress can then display elevated resistance to a subsequent stress of a different type (see text). In some cases no cross-protection is observed. In other cases it is observed, but this cross-protection can be reciprocal or nonreciprocal. This can depend on the nature and dose of the initial and subsequent stress.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0048-2016
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Image of FIGURE 3
FIGURE 3

Exposure to combinatorial stresses can yield nonadditive outputs. Simultaneous exposure to some combinations of stress (i.e., certain combinatorial stresses) can yield additive outputs if there are no significant interactions between the stress pathways that mediate these responses. However, for some combinatorial stresses (see text), stress pathway interference can block the normal response to one of the imposed stresses, leading to combinatorial stress sensitivity. We are unaware of any examples of the opposite effect, where stress pathway enhancement might lead to elevated levels of combinatorial stress resistance.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0048-2016
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Image of FIGURE 4
FIGURE 4

Different aspects of stress adaptation occur over different timescales. This generic figure summarizes this principle of an environmental insult such as osmotic stress (see text). However, some stresses may include adaptation mechanisms that occur over other timescales.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0048-2016
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