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Phylogenetic diversity of stress signalling pathways in fungi.

Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, Brown AJ - BMC Evol. Biol. (2009)

Bottom Line: To test this hypothesis we have compared the conservation of stress signalling molecules in diverse fungal species with their stress resistance.This revealed that in general, central components of the osmotic, oxidative and cell wall stress signalling pathways are relatively well conserved, whereas the sensors lying upstream and transcriptional regulators lying downstream of these modules have diverged significantly.Our data are consistent with the hypothesis that fungal stress signalling components have undergone rapid recent evolution to tune the stress responses in a niche-specific fashion.

View Article: PubMed Central - HTML - PubMed

Affiliation: Aberdeen Fungal Group, School of Medical Sciences, University of Aberdeen, Institute of Medical Sciences, Foresterhill, Aberdeen, AB25 2ZD, UK. e.nikolaou@abdn.ac.uk

ABSTRACT

Background: Microbes must sense environmental stresses, transduce these signals and mount protective responses to survive in hostile environments. In this study we have tested the hypothesis that fungal stress signalling pathways have evolved rapidly in a niche-specific fashion that is independent of phylogeny. To test this hypothesis we have compared the conservation of stress signalling molecules in diverse fungal species with their stress resistance. These fungi, which include ascomycetes, basidiomycetes and microsporidia, occupy highly divergent niches from saline environments to plant or mammalian hosts.

Results: The fungi displayed significant variation in their resistance to osmotic (NaCl and sorbitol), oxidative (H2O2 and menadione) and cell wall stresses (Calcofluor White and Congo Red). There was no strict correlation between fungal phylogeny and stress resistance. Rather, the human pathogens tended to be more resistant to all three types of stress, an exception being the sensitivity of Candida albicans to the cell wall stress, Calcofluor White. In contrast, the plant pathogens were relatively sensitive to oxidative stress. The degree of conservation of osmotic, oxidative and cell wall stress signalling pathways amongst the eighteen fungal species was examined. Putative orthologues of functionally defined signalling components in Saccharomyces cerevisiae were identified by performing reciprocal BLASTP searches, and the percent amino acid identities of these orthologues recorded. This revealed that in general, central components of the osmotic, oxidative and cell wall stress signalling pathways are relatively well conserved, whereas the sensors lying upstream and transcriptional regulators lying downstream of these modules have diverged significantly. There was no obvious correlation between the degree of conservation of stress signalling pathways and the resistance of a particular fungus to the corresponding stress.

Conclusion: Our data are consistent with the hypothesis that fungal stress signalling components have undergone rapid recent evolution to tune the stress responses in a niche-specific fashion.

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Degree of conservation of fungal osmotic stress regulators. (A) Orthologues of S. cerevisiae osmotic stress regulators in the fungi analysed. The organisms are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID across all of the fungal species examined. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of osmotic stress regulators across the fungal species examined based on the model of the osmotic stress pathway in S. cerevisiae described by Krantz and co-workers (2006) [18].
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Figure 3: Degree of conservation of fungal osmotic stress regulators. (A) Orthologues of S. cerevisiae osmotic stress regulators in the fungi analysed. The organisms are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID across all of the fungal species examined. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of osmotic stress regulators across the fungal species examined based on the model of the osmotic stress pathway in S. cerevisiae described by Krantz and co-workers (2006) [18].

Mentions: First, putative orthologues were identified for each S. cerevisiae protein in the other seventeen fungal species by screening for reciprocal best hits, as described in Materials and Methods. Lists of fungal orthologues are presented as additional file 2. Proteins involved in osmotic, oxidative and cell wall stress signalling were then selected, based on recent models of these pathways in S. cerevisiae. We used the model of the osmotic stress signalling pathway reported by Krantz and co-workers (2006) [18], the cell wall stress pathway described by Levin (2005) [25], and a model of the oxidative stress signalling pathway based on the reviews of Moye-Rowley (2003) [19] and Ikner and Shiozaki (2005) [20]. We then examined the conservation of each signalling pathway in each fungus by collating the percent identities for the relevant regulators, relative to their S. cerevisiae orthologues, as reported by BLASTP (Figures 3, 4 and 5). The orthologues are listed in the additional file 2.


Phylogenetic diversity of stress signalling pathways in fungi.

Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, Brown AJ - BMC Evol. Biol. (2009)

Degree of conservation of fungal osmotic stress regulators. (A) Orthologues of S. cerevisiae osmotic stress regulators in the fungi analysed. The organisms are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID across all of the fungal species examined. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of osmotic stress regulators across the fungal species examined based on the model of the osmotic stress pathway in S. cerevisiae described by Krantz and co-workers (2006) [18].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2666651&req=5

Figure 3: Degree of conservation of fungal osmotic stress regulators. (A) Orthologues of S. cerevisiae osmotic stress regulators in the fungi analysed. The organisms are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID across all of the fungal species examined. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of osmotic stress regulators across the fungal species examined based on the model of the osmotic stress pathway in S. cerevisiae described by Krantz and co-workers (2006) [18].
Mentions: First, putative orthologues were identified for each S. cerevisiae protein in the other seventeen fungal species by screening for reciprocal best hits, as described in Materials and Methods. Lists of fungal orthologues are presented as additional file 2. Proteins involved in osmotic, oxidative and cell wall stress signalling were then selected, based on recent models of these pathways in S. cerevisiae. We used the model of the osmotic stress signalling pathway reported by Krantz and co-workers (2006) [18], the cell wall stress pathway described by Levin (2005) [25], and a model of the oxidative stress signalling pathway based on the reviews of Moye-Rowley (2003) [19] and Ikner and Shiozaki (2005) [20]. We then examined the conservation of each signalling pathway in each fungus by collating the percent identities for the relevant regulators, relative to their S. cerevisiae orthologues, as reported by BLASTP (Figures 3, 4 and 5). The orthologues are listed in the additional file 2.

Bottom Line: To test this hypothesis we have compared the conservation of stress signalling molecules in diverse fungal species with their stress resistance.This revealed that in general, central components of the osmotic, oxidative and cell wall stress signalling pathways are relatively well conserved, whereas the sensors lying upstream and transcriptional regulators lying downstream of these modules have diverged significantly.Our data are consistent with the hypothesis that fungal stress signalling components have undergone rapid recent evolution to tune the stress responses in a niche-specific fashion.

View Article: PubMed Central - HTML - PubMed

Affiliation: Aberdeen Fungal Group, School of Medical Sciences, University of Aberdeen, Institute of Medical Sciences, Foresterhill, Aberdeen, AB25 2ZD, UK. e.nikolaou@abdn.ac.uk

ABSTRACT

Background: Microbes must sense environmental stresses, transduce these signals and mount protective responses to survive in hostile environments. In this study we have tested the hypothesis that fungal stress signalling pathways have evolved rapidly in a niche-specific fashion that is independent of phylogeny. To test this hypothesis we have compared the conservation of stress signalling molecules in diverse fungal species with their stress resistance. These fungi, which include ascomycetes, basidiomycetes and microsporidia, occupy highly divergent niches from saline environments to plant or mammalian hosts.

Results: The fungi displayed significant variation in their resistance to osmotic (NaCl and sorbitol), oxidative (H2O2 and menadione) and cell wall stresses (Calcofluor White and Congo Red). There was no strict correlation between fungal phylogeny and stress resistance. Rather, the human pathogens tended to be more resistant to all three types of stress, an exception being the sensitivity of Candida albicans to the cell wall stress, Calcofluor White. In contrast, the plant pathogens were relatively sensitive to oxidative stress. The degree of conservation of osmotic, oxidative and cell wall stress signalling pathways amongst the eighteen fungal species was examined. Putative orthologues of functionally defined signalling components in Saccharomyces cerevisiae were identified by performing reciprocal BLASTP searches, and the percent amino acid identities of these orthologues recorded. This revealed that in general, central components of the osmotic, oxidative and cell wall stress signalling pathways are relatively well conserved, whereas the sensors lying upstream and transcriptional regulators lying downstream of these modules have diverged significantly. There was no obvious correlation between the degree of conservation of stress signalling pathways and the resistance of a particular fungus to the corresponding stress.

Conclusion: Our data are consistent with the hypothesis that fungal stress signalling components have undergone rapid recent evolution to tune the stress responses in a niche-specific fashion.

Show MeSH