Novel Acid Phosphatase in Candida glabrata Suggests Selective Pressure and Niche Specialization in the Phosphate Signal Transduction Pathway
Open accessAbstract
Evolution through natural selection suggests unnecessary genes are lost. We observed that the yeast Candida glabrata lost the gene encoding a phosphate-repressible acid phosphatase (PHO5) present in many yeasts including Saccharomyces cerevisiae. However, C. glabrata still had phosphate starvation-inducible phosphatase activity. Screening a C. glabrata genomic library, we identified CgPMU2, a member of a three-gene family that contains a phosphomutase-like domain. This small-scale gene duplication event could allow for sub- or neofunctionalization. On the basis of phylogenetic and biochemical characterizations, CgPMU2 has neofunctionalized to become a broad range, phosphate starvation-regulated acid phosphatase, which functionally replaces PHO5 in this pathogenic yeast. We determined that CgPmu2, unlike ScPho5, is not able to hydrolyze phytic acid (inositol hexakisphosphate). Phytic acid is present in fruits and seeds where S. cerevisiae grows, but is not abundant in mammalian tissues where C. glabrata grows. We demonstrated that C. glabrata is limited from an environment where phytic acid is the only source of phosphate. Our work suggests that during evolutionary time, the selection for the ancestral PHO5 was lost and that C. glabrata neofunctionalized a weak phosphatase to replace PHO5. Convergent evolution of a phosphate starvation-inducible acid phosphatase in C. glabrata relative to most yeast species provides an example of how small changes in signal transduction pathways can mediate genetic isolation and uncovers a potential speciation gene.
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CgPMU2 transcript levels are lower in high-phosphate conditions and substantially higher during phosphate starvation.
“Consistent with this, CgPMU2 transcript levels were lower in high-phosphate conditions and substantially higher during phosphate starvation [116].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [116]
The C. glabrata genome uniquely codes for a family of three phosphatases, CgPmu1-3, which possess different substrate specificity.
“Instead, C. glabrata genome uniquely codes for a family of three phosphatases, CgPmu1-3 (C. glabrata phosphomutase-like protein 1–3), which possess different substrate specificity [116].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [116]
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 [116]
CgPmu2 is required to grow in the presence of organic phosphate compounds as the sole phosphate source in vitro.
“Although CgPmu2 was required to grow in the presence of organic phosphate compounds as the sole phosphate source in vitro [116], it remains to be determined whether neofunctionalization of the CgPMU gene family confers a growth advantage in the mammalian host.”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [116]
Of the three CgPmu proteins, secreted phosphatase activity of only CgPmu2 is induced in response to phosphate starvation.
“Of three CgPmu proteins, secreted phosphatase activity of only CgPmu2 was induced in response to phosphate starvation [116].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [116]
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- Authors
- Orkwis, B. R., Davies, D. L., Kerwin, C. L., Sanglard, D., & Wykoff, D. D.
- Affiliations
- Villanova University (US)
- Centre Hospitalier Universitaire Vaudois (CH)
- Corresponding author
- Wykoff, Dennis D
- Venue
- Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-11-01
- Volume
- 186
- Issue
- 3
- Pages
- 885-895
- ISSN
- 0016-6731 (ISSN-L)
- 1943-2631
- PMC
- PMC2975289
- OpenAlex
- W2121034527
- Cited by
- 21
- References
- 33
- Citations by year
- 2026: 2 · 2024: 1 · 2023: 2 · 2021: 1 · 2020: 1 · 2019: 2 · 2018: 3 · 2017: 1 · 2016: 2 · 2015: 1 · 2014: 2 · 2013: 1 · 2012: 1
- FWCI
- 0.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Genetics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- National Science Foundation (0747799)
- Villanova University
- Center for Undergraduate Research and Scholarship, Bowling Green State University
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Phytase and its Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Candida glabrata, acid phosphatase, PHO5, neofunctionalization, gene duplication, gene loss, phosphate limitation, phytic acid, convergent evolution, speciation genes, ecological specialization, Saccharomyces cerevisiae
- MeSH terms
- Acid Phosphatase, Amino Acid Sequence, Enzyme Induction, Fungal Proteins, Genes, Fungal, Genetic Complementation Test, Hydrolysis, Molecular Sequence Data, Mutation, Phosphates, Recombinant Fusion Proteins, Selection, Genetic, Substrate Specificity, Signal Transduction, Gene Library, Gene Expression Regulation, Fungal, Open Reading Frames, Sequence Alignment, Evolution, Molecular, Candida glabrata
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