Dynamic changes in yeast phosphatase families allow for specialization in phosphate and thiamine starvation
Open accessAbstract
Abstract Convergent evolution is often due to selective pressures generating a similar phenotype. We observe relatively recent duplications in a spectrum of Saccharomycetaceae yeast species resulting in multiple phosphatases that are regulated by different nutrient conditions – thiamine and phosphate starvation. This specialization is both transcriptional and at the level of phosphatase substrate specificity. In Candida glabrata, loss of the ancestral phosphatase family was compensated by the co-option of a different histidine phosphatase family with three paralogs. Using RNA-seq and functional assays, we identify one of these paralogs, CgPMU3, as a thiamine phosphatase. We further determine that the 81% identical paralog CgPMU2 does not encode thiamine phosphatase activity; however, both are capable of cleaving the phosphatase substrate, 1-napthyl-phosphate. We functionally demonstrate that members of this family evolved novel enzymatic functions for phosphate and thiamine starvation, and are regulated transcriptionally by either nutrient condition, and observe similar trends in other yeast species. This independent, parallel evolution involving two different families of histidine phosphatases suggests that there were likely similar selective pressures on multiple yeast species to recycle thiamine and phosphate. In this work, we focused on duplication and specialization, but there is also repeated loss of phosphatases, indicating that the expansion and contraction of the phosphatase family is dynamic in many Ascomycetes. The dynamic evolution of the phosphatase gene families is perhaps just one example of how gene duplication, co-option, and transcriptional and functional specialization together allow species to adapt to their environment with existing genetic resources.
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C. glabrata appears to have neofunctionalized the CgPmu family to compensate for the loss of the ancestral Pho5 phosphatase.
“Overall, C. glabrata appears to have neofunctionalized the CgPmu family to compensate for the loss of the ancestral Pho5 phosphatase [116,119].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [119]
CgPmu3 is a thiamine phosphatase that is transcriptionally regulated by CgThi3 in response to thiamine starvation.
“Recently, CgPmu3 has been shown to be a thiamine phosphatase that is transcriptionally regulated by the transcription factor CgThi3 in response to thiamine starvation [119].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [119]
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Candida glabrata: pathogenicity and resistance mechanisms for adaptation and survival
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- Authors
- Nahas, J. V., Iosue, C. L., Shaik, N. F., Selhorst, K., He, B. Z., & Wykoff, D. D.
- Affiliations
- Villanova University (US)
- University of Iowa (US)
- Corresponding author
- Wykoff, Dennis D
- Venue
- G3 Genes Genomes Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-07-01
- Volume
- 8
- Issue
- 7
- Pages
- 2333-2343
- ISSN
- 2160-1836 (ISSN-L)
- PMC
- PMC6027888
- OpenAlex
- W2801279350
- Cited by
- 8
- References
- 53
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 1 · 2019: 2
- FWCI
- 0.27
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- G3 Genes Genomes Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (1412582)
- Villanova University
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
- Keywords
- gene duplication, convergent evolution, phosphate limitation, Candida glabrata, Saccharomycetaceae, co-option, functional specialization, transcriptional regulation, 1-naphthyl phosphate, nutrient cycling, gene family expansion and contraction
- MeSH terms
- Saccharomycetales, Environment, Fungal Proteins, Multigene Family, Hydrolysis, Phosphates, Phosphoric Monoester Hydrolases, Phylogeny, Substrate Specificity, Thiamine, Yeasts, Gene Expression Regulation, Fungal, Gene Duplication, Candida glabrata, High-Throughput Nucleotide Sequencing
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