The bZIP Transcription Factor Rca1p Is a Central Regulator of a Novel CO2 Sensing Pathway in Yeast
Open accessAbstract
Like many organisms the fungal pathogen Candida albicans senses changes in the environmental CO(2) concentration. This response involves two major proteins: adenylyl cyclase and carbonic anhydrase (CA). Here, we demonstrate that CA expression is tightly controlled by the availability of CO(2) and identify the bZIP transcription factor Rca1p as the first CO(2) regulator of CA expression in yeast. We show that Rca1p upregulates CA expression during contact with mammalian phagocytes and demonstrate that serine 124 is critical for Rca1p signaling, which occurs independently of adenylyl cyclase. ChIP-chip analysis and the identification of Rca1p orthologs in the model yeast Saccharomyces cerevisiae (Cst6p) point to the broad significance of this novel pathway in fungi. By using advanced microscopy we visualize for the first time the impact of CO(2) build-up on gene expression in entire fungal populations with an exceptional level of detail. Our results present the bZIP protein Rca1p as the first fungal regulator of carbonic anhydrase, and reveal the existence of an adenylyl cyclase independent CO(2) sensing pathway in yeast. Rca1p appears to regulate cellular metabolism in response to CO(2) availability in environments as diverse as the phagosome, yeast communities or liquid culture.
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In other fungal species, bicarbonate plays critical roles in energy metabolism and morphogenesis through the cAMP/PKA signaling pathway that converges at the regulator Efg1.
“In other fungal species, bicarbonate plays critical roles in energy metabolism and morphogenesis, as it is acting through the cyclic adenosine monophosphate–dependent protein kinase A (cAMP/PKA) signaling pathway that converges at the regulator Efg1 (refs. 23–25).”
From Candida auris skin tropism and antifungal resistance are mediated by carbonic anhydrase Nce103 (2025) · cites this paper as [24]
The Introduction and Figure 8 in the Discussion describe bicarbonate as important for fungal metabolism and show bicarbonate regulating morphogenesis through adenylyl cyclase and cAMP/PKA. Figure 8 depicts metabolism as a separate pathway, however, and no passage found identifies Efg1 as a point of convergence (searched: Efg1). The source therefore does not support the claim that both roles act through cAMP/PKA and converge at Efg1. Page numbers are unavailable in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredNce103 regulates mitochondrial functions through the cAMP-PKA-Efg1 signalling.
“it regulates mitochondrial functions through the cAMP–PKA–Efg1 signalling24,48,49.”
From Candida auris skin tropism and antifungal resistance are mediated by carbonic anhydrase Nce103 (2025) · cites this paper as [24]
The Discussion (page unavailable) suggests that carbonic anhydrase, Nce103, could indirectly affect differentiation through the cAMP-PKA pathway. It does not say that Nce103 regulates mitochondrial functions or identify Efg1 as part of that effect. The paper also reports that CO₂ regulation of NCE103 expression is independent of cAMP signaling. (LLM, conf=0.78)
Experimental — accuracy not yet measuredLevels of CO2/HCO3− readily diffuse across cell membranes to moderate intracellular pH, act as metabolic inhibitors, may induce complex transcriptional responses, and signal other critical reactions.
“Besides the role of CO2 in affecting medium acid-base chemistry, levels of CO2/HCO3 − readily diffuse across cell membranes to moderate intracellular pH (Gutknecht et al., 1977), act as metabolic inhibitors, and may induce complex transcriptional responses (Cottier et al., 2012; Follonier et al., 2013), and signal other critical reactions (see, Blombach and Takors, 2015).”
From Toward Best Practices for Controlling Mammalian Cell Culture Environments (2022) · cites this paper as Cottier et al., 2012
The Discussion (page not provided) reports that CO2 changes carbonic anhydrase expression through a transcription-factor-mediated pathway in yeast, supporting the cited claim about transcriptional responses. The Introduction describes CO2/HCO3− as important to fungal metabolism, but the passages do not support the adjacent claim that they act as metabolic inhibitors. The membrane-diffusion and other-signalling clauses have separate citations in the citing sentence. (LLM, conf=0.82)
Experimental — accuracy not yet measuredA CSP is well documented in other fungal species.
“a CSP is well documented in other fungal species24,28,29,48,50”
From Candida auris skin tropism and antifungal resistance are mediated by carbonic anhydrase Nce103 (2025) · cites this paper as [24]
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Candida auris skin tropism and antifungal resistance are mediated by carbonic anhydrase Nce103
Phan-Canh, T., Coman, C., Lackner, M., Troppmair, N., Müller, C., Cerbu, D., Seiser, S., Penninger, P., Tsymala, I., Khunweeraphong, N., et al. (2025) · Nature Microbiology · doi:10.1038/s41564-025-02189-z · Cited by 16 · see citing works
“Although a CSP is well documented in other fungal species 24,28,29,48,50 , its unique role in promoting AMB R has not been demonstrated.”
A CO <sub>2</sub> sensing module modulates β-1,3-glucan exposure in <i>Candida albicans</i>
Avelar, G. M., Pradhan, A., Ma, Q., Hickey, E., Leaves, I., Liddle, C., Rodriguez Rondon, A. V., Kaune, A.-K., Shaw, S., Maufrais, C., et al. (2024) · mBio · doi:10.1128/mbio.01898-23 · Cited by 15 · see citing works
Cheon, S. A., Thak, E. J., Bahn, Y., & Kang, H. A. (2017) · Scientific Reports · doi:10.1038/s41598-017-04290-8 · Cited by 15 · see citing works
Host Sensing by Pathogenic Fungi
Sherrington, S. L., Kumwenda, P., Kousser, C., & Hall, R. A. (2017) · Advances in applied microbiology · doi:10.1016/bs.aambs.2017.10.004 · Cited by 13 · see citing works
Mechanisms of Drug Resistance in Fungi and Their Significance in Biofilms
Prasad, R., Shah, A. H., & Dhamgaye, S. (2014) · Springer series on biofilms · doi:10.1007/978-3-642-53833-9_4 · Cited by 13 · see citing works
Fungal Carbonic Anhydrases and Their Inhibition
Lehneck, R., & Pöggeler, S. (2016) · Topics in medicinal chemistry · doi:10.1007/7355_2016_10 · Cited by 7 · see citing works
Cellular Localization of Carbonic Anhydrase Nce103p in Candida albicans and Candida parapsilosis
Dostál, J., Bláha, J., Hadravová, R., Hubálek, M., Hrušková‐Heidingsfeldová, O., & Pichová, I. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030850 · Cited by 7 · see citing works
Analysis of Pneumocystis Transcription Factor Evolution and Implications for Biology and Lifestyle
Ames, R. M., Brown, A. J. P., Gudelj, I., & Nev, O. A. (2023) · mBio · doi:10.1128/mbio.02711-22 · Cited by 7 · see citing works
Miao, Q., Wang, Z., Yin, Z., Liu, X., Li, R., Zhang, K., & Li, J. (2023) · Science China Life Sciences · doi:10.1007/s11427-022-2300-2 · Cited by 5 · see citing works
Shah, A., & Eikmanns, B. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154382 · Cited by 4 · see citing works
Carbonic anhydrases from pathogens
Bonardi, A., Gratteri, P., & Nocentini, A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816476-1.00019-8 · Cited by 4 · see citing works
Proteome analysis of Candida albicans cells undergoing chlamydosporulation
Ingle, S., Kazi, R. S., Patil, R., & Zore, G. B. (2019) · Journal of Proteins and Proteomics · doi:10.1007/s42485-019-00024-8 · Cited by 4 · see citing works
Carbon Dioxide Controls Fungal Fitness and Skin Tropism of Candida aurisPreprint
Phan-Canh, T., Penninger, P., Seiser, S., Khunweeraphong, N., Moser, D., Bitencourt, T. A., Arzani, H., Chen, W., Zenz, L.-M., Knarr, A., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.12.589292 · Cited by 4 · see citing works
Carbon dioxide suppresses filamentous growth in the human fungal pathogen Candida tropicalis
Yue, H., Hu, J., Xu, X., & Liu, Q. (2024) · Microbial Pathogenesis · doi:10.1016/j.micpath.2024.107255 · Cited by 1 · see citing works
CO2 influences amphotericin B resistance and Candida auris colonization
Balakumar, A., & Thangamani, S. (2026) · Trends in Microbiology · doi:10.1016/j.tim.2026.02.009
Mello, T. R. C., Ramos, L. S., Branquinha, M. H., & Santos, A. L. S. (2026) · Medical Gas Research · doi:10.4103/mgr.medgasres-d-26-00038
Li, Y., She, Y., Wang, T., Liu, Y., Wang, S., Hu, S., Liu, C. X., & Dang, Y. (2026) · Journal of Fungi · doi:10.3390/jof12080555
- Authors
- Cottier, F., Raymond, M., Kurzai, O., Bolstad, M., Leewattanapasuk, W., Jiménez-López, C., Lorenz, M. C., Sanglard, D., Váchová, L., Pavelka, N., Palková, Z., & Mühlschlegel, F. A.
- Affiliations
- University of Kent (GB)
- Institute for Research in Immunology and Cancer (CA)
- Leibniz-Institut für Naturstoff-Forschung und Infektionsbiologie e. V. - Hans-Knöll-Institut (HKI) (DE)
- The University of Texas Health Science Center at Houston (US)
- University of Lausanne (CH)
- Charles University (CZ)
- Agency for Science, Technology and Research (SG)
- Corresponding author
- Mühlschlegel, Fritz A.
- ORCID
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-01-12
- Volume
- 8
- Issue
- 1
- Pages
- e1002485
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC3257301
- OpenAlex
- W2002950258
- Cited by
- 55
- References
- 47
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 2 · 2022: 1 · 2021: 1 · 2020: 2 · 2019: 2 · 2018: 3 · 2017: 6 · 2016: 5 · 2015: 4 · 2014: 6 · 2013: 7 · 2012: 7
- FWCI
- 3.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- ASEP (submittedVersion, public-domain)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Kent Academic Repository (University of Kent) (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion, other-oa)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (AV0Z50200510)
- Canadian Institutes of Health Research (84341_1)
- Medical Research Council
- Biotechnology and Biological Sciences Research Council
- National Institute of Allergy and Infectious Diseases (R01AI075091, R21AI071134)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Enzyme function and inhibition
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- bZIP transcription factors, carbon dioxide detection, carbonic anhydrase, Candida albicans, phagosome, Saccharomyces cerevisiae, gene expression regulation, fungal metabolism, yeast communities
- MeSH terms
- Adenosine Triphosphatases, Carbon Dioxide, Environment, Metalloendopeptidases, Microbiological Techniques, Models, Biological, Phagosomes, Saccharomyces cerevisiae, Yeasts, Signal Transduction, Gene Expression Regulation, Fungal, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mitochondrial Proteins, Saccharomyces cerevisiae Proteins, Organisms, Genetically Modified, Chromatin Immunoprecipitation, Basic-Leucine Zipper Transcription Factors, Quorum Sensing, Biota
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