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Phylogenetic diversity of stress signalling pathways in fungi
Open accessAbstract
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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![Figure 1 Neighbour-joining phylogeny constructed using a concatenated alignment of 8 genes for each of the 18 fungal species. Bootstrap scores for all the nodes are displayed. Encephalitozoon cuniculi was selected as an outgroup. The basidiomycetes and ascomycetes form distinct clades. Dotted lines indicate yeast-like fungi, thick straight lines indicate filamentous fungi, whereas dashed lines indicate dimorphic fungi [information adapted [144]]: red, human pathogens; green, plant pathogens; blue, benign fungi. Scale bar corresponds to 0.05 amino acid changes/site.](/paper-figures/64316cf6404a46b5b26c54996d10c7ab/phylogenetic-diversity-of-stress-signalling-pathways-in-fungi-figure-1.jpg)
![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].](/paper-figures/0053bfb4923a4a03bb102dc3fa4742dd/phylogenetic-diversity-of-stress-signalling-pathways-in-fungi-figure-3.jpg)
![Figure 4 Degree of conservation of fungal oxidative stress regulators. (A) Orthologues of S. cerevisiae oxidative stress regulators in the fungi analysed. As before, the fungi are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of oxidative stress regulators across the fungal species examined based on the S. cerevisiae oxidative stress pathway adapted from reviews by Moye-Rowley (2003) [19] and Ikner and Shiozaki (2005) [20].](/paper-figures/917d96b1abcd41d298a9dc13b248d508/phylogenetic-diversity-of-stress-signalling-pathways-in-fungi-figure-4.jpg)
![Figure 5 Degree of conservation of fungal cell wall stress regulators. (A) Orthologues of S. cerevisiae cell wall stress regulators in the fungi analysed. As before, the fungi are ordered according to their position in the phylogeny, and the regulators ordered according to their mean %ID. Closed indicates no orthologue identified. (B) Mean conservation (%ID) of cell wall stress regulators across the fungal species examined based on the S. cerevisiae cell wall stress pathway adapted from Levin (2005) [25].](/paper-figures/e3d5064024a14e84816e0c646c75ae37/phylogenetic-diversity-of-stress-signalling-pathways-in-fungi-figure-5.jpg)
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“C. glabrata is highly tolerant to oxidative, cell wall, osmotic and endoplasmic reticulum (ER) stress [79].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [79]
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“For example, an experimental E. coli culture could evolve the ability to aerobically utilize citrate [37], or the ability to use the non-natural carbon source 1,2-propanediol [71]; also, a strain deficient in glutathione biosynthesis was able to develop compensatory mutations to restore this function [147].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [147]
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Cites
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Assessment of the metabolome in genomically diverse Candida albicans isolates
Alaban, L. R. (2022) · theses.fr (ABES) · doi:10.70675/6127ebd7z2b67z4728z960dzdc64762b4c70
Campanella, J. E. M., Barbugli, P. A., Gomes, A. A. S., Freitas, F. Z., Malavazi, I., & Bertolini, M. C. (2026) · FEBS Journal · doi:10.1111/febs.70643
Haroun, M., Addala, S., BOUHDJER, M. L., Bouhdjer, A., Abdelouahed, K., Selmi, N., Sahnoune, D., & Bouhdjer, L. (2026) · Ceramics International · doi:10.1016/j.ceramint.2026.07.559
Schruefer, S., Hu, Y., & Ebel, F. (2026) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuag037
Neumann, C., Bielčik, M., & Rillig, M. C. (2026) · Fungal ecology · doi:10.1016/j.funeco.2026.101541
Gómez-Gaviria, M., Ramírez-Sotelo, U., & Mora-Montes, H. M. (2026) · Journal of Fungi · doi:10.3390/jof12100791
Metadata
- Authors
- Nikolaou, E., Agrafioti, I., Stumpf, M., Quinn, J., Stansfield, I., & Brown, A. J.
- Affiliations
- University of Aberdeen (GB)
- Imperial College London (GB)
- Newcastle University (GB)
- Corresponding author
- Brown, Alistair JP
- Venue
- BMC Evolutionary Biology
- Published
- 2009-02-21
- Volume
- 9
- Issue
- 1
- Pages
- 44-44
- ISSN
- 1471-2148 (ISSN-L)
- PMC
- PMC2666651
- OpenAlex
- W1985831723
- Cited by
- 206
- References
- 159
- Citations by year
- 2026: 12 · 2025: 13 · 2024: 7 · 2023: 9 · 2022: 9 · 2021: 7 · 2020: 14 · 2019: 13 · 2018: 8 · 2017: 13 · 2016: 15 · 2015: 17 · 2014: 18 · 2013: 16 · 2012: 13
- FWCI
- 4.69
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Evolutionary Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- Wellcome Trust (080088)
- University of Exeter
- Imperial College London
- University of Aberdeen
- Biotechnology and Biological Sciences Research Council (BB/D009308/1, BB/C510391/1, BB/F00513X/1, BB/F013566/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- stress tolerance, osmotic stress, oxidative stress, cell wall stress, phylogenetic conservation, orthologs, human fungal pathogens, plant pathogenic fungi, Candida albicans, Ascomycota, Basidiomycota, microsporidia, signal transduction
- MeSH terms
- Benzenesulfonates, Candida albicans, Cell Wall, Congo Red, DNA, Fungal, Fungal Proteins, Hydrogen Peroxide, Osmotic Pressure, Phylogeny, Saccharomyces cerevisiae, Sodium Chloride, Sorbitol, Signal Transduction, Gene Expression Regulation, Fungal, Genome, Fungal, Oxidative Stress, Evolution, Molecular, Vitamin K 3
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