The fungal pathogen Candida glabrata does not depend on surface ferric reductases for iron acquisition
Open accessAbstract
Iron acquisition is a crucial virulence determinant for many bacteria and fungi, including the opportunistic fungal pathogens Candida albicans and C. glabrata. While the diverse strategies used by C. albicans for obtaining iron from the host are well-described, much less is known about the acquisition of this micronutrient from host sources by C. glabrata – a distant relative of C. albicans with closer evolutionary ties to Saccharomyces cerevisiae, which nonetheless causes severe clinical symptoms in humans. Here we show that C. glabrata is much more restricted than C. albicans in using host iron sources, lacking, for example, the ability to grow on transferrin and hemin/hemoglobin. Instead, C. glabrata is able to use ferritin and non-protein-bound iron (FeCl3) as iron sources in a pH-dependent manner. As in other fungal pathogens, iron-dependent growth requires the reductive high affinity (HA)-iron uptake system. Typically highly conserved, this uptake mechanism normally relies on initial ferric reduction by cell-surface ferric reductases. The C. glabrata genome contains only three such putative ferric reductases, which were found to be dispensable for iron-dependent growth. In addition and in contrast to C. albicans and S. cerevisiae, we also detected no surface ferric reductase activity in C. glabrata. Instead, extracellular ferric reduction was found in this and the two other fungal species, which was largely dependent on an excreted low-molecular weight, non-protein ferric reductant. We therefore propose an iron acquisition strategy of C. glabrata which differs from other pathogenic fungi, such as C. albicans, in that it depends on a limited set of host iron sources and that it lacks the need for surface ferric reductases. Extracellular ferric reduction by a secreted molecule possibly compensates for the loss of surface ferric reductase activity in the HA-iron uptake system.
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Putative CFEM domain-containing protein CgCcw14, haem oxygenase CgHmx1, and intracellular iron trafficking machinery components including vacuolar and mitochondrial iron transporters have been identified in C. glabrata.
“Recently, putative cell surface-associated, cysteine-rich Common in Fungal Extracellular Membrane (CFEM) domain-containing protein (CgCcw14), haem oxygenase (CgHmx1) and intracellular iron trafficking machinery components including vacuolar (CgCcc1, CgSmf1, CgSmf3, and CgFth1) and mitochondrial (CgMmt1, CgMmt2, CgAtm1, CgMrs3, and CgMrs4) iron transporters have been identified in C. glabrata [122,”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [125]
C. glabrata is unable to utilize the host iron proteins haemoglobin and transferrin as iron sources.
“C. glabrata is also unable to utilize the host iron proteins, haemoglobin, and transferrin, as iron sources [125].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [125]
C. glabrata could utilize ferritin and ferric chloride as iron sources in a pH-dependent manner via the reductive high-affinity iron uptake system.
“C. glabrata could also utilize ferritin and ferric chloride as iron sources in a pH-dependent manner via reductive high-affinity iron uptake system [125].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [125]
Despite the presence of three ferric reductase genes, C. glabrata exhibited no surface ferric reductase activity.
“Despite the presence of three ferric reductase genes, C. glabrata exhibited no surface ferric reductase activity, and it has been postulated that extracellular ferric reduction may be achieved through a secreted molecule [125].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [125]
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Gerwien, F., Skrahina, V., Kasper, L., Hube, B., & Brunke, S. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux050 · Cited by 246 · see citing works
Self-citationCandida albicans and Candida glabrata : global priority pathogens
Katsipoulaki, M., Stappers, M. H. T., Malavia, D., Brunke, S., Hube, B., & Gow, N. A. R. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00021-23 · Cited by 174 · see citing works
Self-citationCandida glabrata: A Lot More Than Meets the Eye
Kumar, K., Askari, F., Sahu, M. S., & Kaur, R. (2019) · Microorganisms · doi:10.3390/microorganisms7020039 · Cited by 128 · see citing works
How the rock-inhabiting fungus K. petricola A95 enhances olivine dissolution through attachment
Gerrits, R., Pokharel, R., Breitenbach, R., Radnik, J., Feldmann, I., Schuessler, J. A., von Blanckenburg, F., Gorbushina, A. A., & Jacques Schott, A. (2020) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2020.05.010 · Cited by 63 · see citing works
Adaptation to iron deficiency in human pathogenic fungi
Martínez‐Pastor, M. T., & Puig, S. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118797 · Cited by 46 · see citing works
Stanford, F. A., & Voigt, K. (2020) · Genes · doi:10.3390/genes11111296 · Cited by 43 · see citing works
Kim, M., Cho, Y., Park, M., Choi, Y., Hwang, S. Y., & Jung, W. H. (2018) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.1810.10019 · Cited by 40 · see citing works
Regulatory and pathogenic mechanisms in response to iron deficiency and excess in fungi
Pijuan, J., Moreno, D. F., Yahya, G., Moisa, M., Ul Haq, I., Krukiewicz, K., Mosbah, R., Metwally, K., & Cavalu, S. (2023) · Microbial Biotechnology · doi:10.1111/1751-7915.14346 · Cited by 37 · see citing works
The regulation of iron homeostasis in the fungal human pathogen Candida glabrata
Devaux, F., & Thiébaut, A. (2019) · Microbiology · doi:10.1099/mic.0.000807 · Cited by 29 · see citing works
Chakraborty, T., Tóth, Z., Tóth, R., Vágvölgyi, C., & Gácser, A. (2020) · mSphere · doi:10.1128/msphere.00227-20 · Cited by 28 · see citing works
Human albumin enhances the pathogenic potential of Candida glabrata on vaginal epithelial cells
Pekmezovic, M. G., Kaune, A.-K., Austermeier, S., Hitzler, S. U. J., Mogavero, S., Hovhannisyan, H., Gabaldón, T., Gresnigt, M. S., & Hube, B. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1010037 · Cited by 19 · see citing works
Self-citationThe intricate link between iron, mitochondria and azoles in Candida species
Genechten, W. V., Vergauwen, R., & Dijck, P. V. (2023) · FEBS Journal · doi:10.1111/febs.16977 · Cited by 19 · see citing works
Delaney, C., Alapati, S., Alshehri, M., Kubalová, D., Veena, C. L. R., Abusrewil, S., Short, B., Bradshaw, D. J., & Brown, J. L. (2023) · Apmis · doi:10.1111/apm.13327 · Cited by 13 · see citing works
Amsri, A., Pruksaphon, K., Thammasit, P., Nosanchuk, J. D., & Youngchim, S. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1367656 · Cited by 12 · see citing works
Oluyele, O., Oladunmoye, M. K., Ogundare, A. O., Onifade, A. K., & Okunnuga, N. A. (2023) · Microbes Infection and Chemotherapy · doi:10.54034/mic.e1961 · Cited by 11 · see citing works
Denecker, T., Li, Y. Z., Fairhead, C., Budin, K., Camadro, J., Bolotin‐Fukuhara, M., Angoulvant, A., & Lelandais, G. (2020) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqaa027 · Cited by 11 · see citing works
Tonmoy, M. I. Q., Ahmed, S. F., Hami, I., Shakil, S. K., Verma, A. K., Hasan, M., Reza, H. A., Bahadur, N. M., Rahaman, M. M., & Hossain, M. S. (2022) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2022.105385 · Cited by 13 · see citing works
Zheng, D., Zhang, X., Ding, J., Yue, D., Yang, F., & Li, Y. (2025) · Critical reviews in microbiology · doi:10.1080/1040841x.2025.2510256 · Cited by 10 · see citing works
Zheng, D., Yue, D., Shen, J., Li, D., Song, Z., Huang, Y., Yong, J., & Li, Y. (2023) · Journal of Applied Microbiology · doi:10.1093/jambio/lxad276 · Cited by 10 · see citing works
Mrs4 loss of function in fungi during adaptation to the cystic fibrosis lung
Murante, D., Demers, E. G., Kurbessoian, T., Ruzic, M., Ashare, A., Stajich, J., & Hogan, D. A. (2023) · mBio · doi:10.1128/mbio.01171-23 · Cited by 8 · see citing works
Benchouaia, M., Ripoche, H., Sissoko, M., Thiébaut, A., Merhej, J., Delaveau, T., Fasseu, L., Benaissa, S., Lorieux, G., Jourdren, L., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02689 · Cited by 8 · see citing works
Sahu, M. S., Purushotham, R., & Kaur, R. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1011281 · Cited by 6 · see citing works
The Effects of Iron Rust on the Ageing of Woods and Their Derived Pulp Paper
Elgat, W. A. A. A., Taha, A. S., Salem, M. Z. M., Fares, Y. G. D., Böhm, M., Mohamed, M. F., Nasser, R. A.-S., & Pommer, V. (2021) · Polymers · doi:10.3390/polym13203483 · Cited by 6 · see citing works
Phosphatidylinositol 3-phosphate regulates iron transport via PI3P-binding CgPil1 protein
Askari, F., Vasavi, B., & Kaur, R. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112855 · Cited by 4 · see citing works
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Kineochelins - a novel group of siderophores from an Antarctic bacteriumPreprint
Králová, S., Spacek, P., Gafriller, J., Bezdíček, M., Medvedcova, V., Séneca, J., Osvatic, J., Grienke, U., Rattei, T., Sekurova, O. N., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.23.707395
Characterization of the nuclear RNase P of Candida glabrata and improvement of genome editing tools
Dahman, Y. (2018) · theses.fr (ABES) · doi:10.70675/82cd4f14z1fe3z42dczaf17z642b31bd4dd1
Transcriptional networks of the stress responses in the human pathogen Candida glabrata
Thiébaut, A. (2018) · theses.fr (ABES) · doi:10.70675/323c74a8z1ae4z4123za081zd0af3ecf65ae
Kineochelins—A New Group of Siderophores From an Antarctic Bacterium
Králová, S., Spacek, P., Gafriller, J., Bezdíček, M., Medvedcova, V., Séneca, J., Osvatic, J., Grienke, U., Rattei, T., Sekurova, O. N., et al. (2026) · Microbial Biotechnology · doi:10.1111/1751-7915.70386
Gómez-Gaviria, M., Ramírez-Sotelo, U., & Mora-Montes, H. M. (2026) · Journal of Fungi · doi:10.3390/jof12100791
- Authors
- Gerwien, F., Safyan, A., Wisgott, S., Brunke, S., Kasper, L., & Hube, B.
- Affiliations
- Leibniz-Institut für Naturstoff-Forschung und Infektionsbiologie e. V. - Hans-Knöll-Institut (HKI) (DE)
- Jena University Hospital (DE)
- Corresponding author
- Kasper, Lydia
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2017-06-08
- Volume
- 8
- Pages
- 1055-1055
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC5463049
- OpenAlex
- W2624428734
- Cited by
- 33
- References
- 94
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 3 · 2023: 8 · 2022: 1 · 2021: 3 · 2020: 6 · 2019: 2 · 2018: 4 · 2017: 1
- FWCI
- 2.74
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Microbiology (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
- Deutsche Forschungsgemeinschaft (SPP 1580, HU 528/16-2, 01EO1002)
- Bundesministerium für Bildung und Forschung (01EO1002)
- International Leibniz Research School for Microbial and Biomolecular Interactions
- Leibniz-Gemeinschaft
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- Candida glabrata, iron acquisition, ferric reductase, high-affinity iron uptake, ferritin, transferrin, hemin, hemoglobin, opportunistic fungal pathogens, Candida albicans comparison
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