Multi trace element profiling in pathogenic and non-pathogenic fungi

Silvia Wehmeier; Emma Morrison; Anthony Plato; Andrea Raab; Jörg Feldmann; Tina Bedekovic; Duncan Wilson; Alexandra C. Brand

doi:10.1016/j.funbio.2020.03.001

Multi trace element profiling in pathogenic and non-pathogenic fungi

Silvia Wehmeier, Emma Morrison, Anthony Plato, Andrea Raab, Jörg Feldmann, Tina Bedekovic, Duncan Wilson, Alexandra C. Brand^* (Corresponding Author)

^*Corresponding author for this work

University of Exeter

Research output: Contribution to journal › Article › peer-review

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Abstract

Maintaining appropriate levels of trace elements during infection of a host is essential for microbial pathogenicity. Here we compared the uptake of 10 trace elements from 3 commonly-used laboratory media by 3 pathogens, Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus, and a model yeast, Saccharomyces cerevisiae. The trace element composition of the yeasts, C. albicans, C. neoformans and S. cerevisiae, grown in rich (YPD) medium, differed primarily in P, S, Fe, Zn and Co. Speciation analysis of the intracellular fraction, which indicates the size of the organic ligands with which trace elements are complexed, showed that the ligands for S were similar in the three fungi but there were significant differences in binding partners for Fe and Zn between C. neoformans and S. cerevisiae. The profile for Cu varied across the 3 yeast species. In a comparison of C. albicans and A. fumigatus hyphae, the former showed higher Fe, Cu, Zn and Mn, while A. fumigatus contained higher P, S Ca and Mo. Washing C. albicans cells with the cell-impermeable chelator, EGTA, depleted 50–90 % of cellular Ca, suggesting that a large proportion of this cation is stored in the cell wall. Treatment with the cell wall stressor, Calcofluor White (CFW), alone had little effect on the elemental profile whilst combined Ca + CFW stress resulted in high cellular Cu and very high Ca. Together our data enhance our understanding of trace element uptake by pathogenic fungi and provide evidence for the cell wall as an important storage organelle for Ca.

Original language	English
Pages (from-to)	516-524
Number of pages	9
Journal	Fungal Biology
Volume	124
Issue number	5
Early online date	10 Mar 2020
DOIs	https://doi.org/10.1016/j.funbio.2020.03.001
Publication status	Published - May 2020

Bibliographical note

Acknowledgements

SW and EM were funded by an MRC NIRG to AB (G0900211/90671). AP was funded by a British Mycological Society Summer Studentship. AB was funded by a Royal Society URF (UF080611) and a Senior Wellcome Research Fellowship (206412/A/17/Z), which also funded TB. DW was funded by a Senior Wellcome Research Fellowship (214317/A/18/Z). The work was carried out in the MRC Centre for Medical Mycology (MR/N006364/2). This article is part of the Fungal Adaptation to Hostile Challenges special issue for the third International Symposium on Fungal Stress (ISFUS), which is supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo grant 2018/20571-6 and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior grant 88881.289327/2018-01.

Keywords

Calcium
Candida albicans
Fungal cell wall
PROTEIN
TOLERANCE
VIRULENCE
ZINC
CANDIDA-ALBICANS
GENE
CALCIUM
GROWTH
RESISTANCE
CALCINEURIN

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

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title = "Multi trace element profiling in pathogenic and non-pathogenic fungi",

abstract = "Maintaining appropriate levels of trace elements during infection of a host is essential for microbial pathogenicity. Here we compared the uptake of 10 trace elements from 3 commonly-used laboratory media by 3 pathogens, Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus, and a model yeast, Saccharomyces cerevisiae. The trace element composition of the yeasts, C. albicans, C. neoformans and S. cerevisiae, grown in rich (YPD) medium, differed primarily in P, S, Fe, Zn and Co. Speciation analysis of the intracellular fraction, which indicates the size of the organic ligands with which trace elements are complexed, showed that the ligands for S were similar in the three fungi but there were significant differences in binding partners for Fe and Zn between C. neoformans and S. cerevisiae. The profile for Cu varied across the 3 yeast species. In a comparison of C. albicans and A. fumigatus hyphae, the former showed higher Fe, Cu, Zn and Mn, while A. fumigatus contained higher P, S Ca and Mo. Washing C. albicans cells with the cell-impermeable chelator, EGTA, depleted 50–90 % of cellular Ca, suggesting that a large proportion of this cation is stored in the cell wall. Treatment with the cell wall stressor, Calcofluor White (CFW), alone had little effect on the elemental profile whilst combined Ca + CFW stress resulted in high cellular Cu and very high Ca. Together our data enhance our understanding of trace element uptake by pathogenic fungi and provide evidence for the cell wall as an important storage organelle for Ca.",

keywords = "Calcium, Candida albicans, Fungal cell wall, PROTEIN, TOLERANCE, VIRULENCE, ZINC, CANDIDA-ALBICANS, GENE, CALCIUM, GROWTH, RESISTANCE, CALCINEURIN",

author = "Silvia Wehmeier and Emma Morrison and Anthony Plato and Andrea Raab and J{\"o}rg Feldmann and Tina Bedekovic and Duncan Wilson and Brand, {Alexandra C.}",

note = "Acknowledgements SW and EM were funded by an MRC NIRG to AB (G0900211/90671). AP was funded by a British Mycological Society Summer Studentship. AB was funded by a Royal Society URF (UF080611) and a Senior Wellcome Research Fellowship (206412/A/17/Z), which also funded TB. DW was funded by a Senior Wellcome Research Fellowship (214317/A/18/Z). The work was carried out in the MRC Centre for Medical Mycology (MR/N006364/2). This article is part of the Fungal Adaptation to Hostile Challenges special issue for the third International Symposium on Fungal Stress (ISFUS), which is supported by the Funda{\c c}{\~a}o de Amparo {\`a} Pesquisa do Estado de S{\~a}o Paulo grant 2018/20571-6 and the Coordena{\c c}{\~a}o de Aperfei{\c c}oamento de Pessoal de N{\'i}vel Superior grant 88881.289327/2018-01.",

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doi = "10.1016/j.funbio.2020.03.001",

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AU - Wehmeier, Silvia

AU - Morrison, Emma

AU - Plato, Anthony

AU - Raab, Andrea

AU - Feldmann, Jörg

AU - Bedekovic, Tina

AU - Wilson, Duncan

AU - Brand, Alexandra C.

N1 - Acknowledgements SW and EM were funded by an MRC NIRG to AB (G0900211/90671). AP was funded by a British Mycological Society Summer Studentship. AB was funded by a Royal Society URF (UF080611) and a Senior Wellcome Research Fellowship (206412/A/17/Z), which also funded TB. DW was funded by a Senior Wellcome Research Fellowship (214317/A/18/Z). The work was carried out in the MRC Centre for Medical Mycology (MR/N006364/2). This article is part of the Fungal Adaptation to Hostile Challenges special issue for the third International Symposium on Fungal Stress (ISFUS), which is supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo grant 2018/20571-6 and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior grant 88881.289327/2018-01.

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N2 - Maintaining appropriate levels of trace elements during infection of a host is essential for microbial pathogenicity. Here we compared the uptake of 10 trace elements from 3 commonly-used laboratory media by 3 pathogens, Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus, and a model yeast, Saccharomyces cerevisiae. The trace element composition of the yeasts, C. albicans, C. neoformans and S. cerevisiae, grown in rich (YPD) medium, differed primarily in P, S, Fe, Zn and Co. Speciation analysis of the intracellular fraction, which indicates the size of the organic ligands with which trace elements are complexed, showed that the ligands for S were similar in the three fungi but there were significant differences in binding partners for Fe and Zn between C. neoformans and S. cerevisiae. The profile for Cu varied across the 3 yeast species. In a comparison of C. albicans and A. fumigatus hyphae, the former showed higher Fe, Cu, Zn and Mn, while A. fumigatus contained higher P, S Ca and Mo. Washing C. albicans cells with the cell-impermeable chelator, EGTA, depleted 50–90 % of cellular Ca, suggesting that a large proportion of this cation is stored in the cell wall. Treatment with the cell wall stressor, Calcofluor White (CFW), alone had little effect on the elemental profile whilst combined Ca + CFW stress resulted in high cellular Cu and very high Ca. Together our data enhance our understanding of trace element uptake by pathogenic fungi and provide evidence for the cell wall as an important storage organelle for Ca.

AB - Maintaining appropriate levels of trace elements during infection of a host is essential for microbial pathogenicity. Here we compared the uptake of 10 trace elements from 3 commonly-used laboratory media by 3 pathogens, Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus, and a model yeast, Saccharomyces cerevisiae. The trace element composition of the yeasts, C. albicans, C. neoformans and S. cerevisiae, grown in rich (YPD) medium, differed primarily in P, S, Fe, Zn and Co. Speciation analysis of the intracellular fraction, which indicates the size of the organic ligands with which trace elements are complexed, showed that the ligands for S were similar in the three fungi but there were significant differences in binding partners for Fe and Zn between C. neoformans and S. cerevisiae. The profile for Cu varied across the 3 yeast species. In a comparison of C. albicans and A. fumigatus hyphae, the former showed higher Fe, Cu, Zn and Mn, while A. fumigatus contained higher P, S Ca and Mo. Washing C. albicans cells with the cell-impermeable chelator, EGTA, depleted 50–90 % of cellular Ca, suggesting that a large proportion of this cation is stored in the cell wall. Treatment with the cell wall stressor, Calcofluor White (CFW), alone had little effect on the elemental profile whilst combined Ca + CFW stress resulted in high cellular Cu and very high Ca. Together our data enhance our understanding of trace element uptake by pathogenic fungi and provide evidence for the cell wall as an important storage organelle for Ca.

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KW - Fungal cell wall

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KW - TOLERANCE

KW - VIRULENCE

KW - ZINC

KW - CANDIDA-ALBICANS

KW - GENE

KW - CALCIUM

KW - GROWTH

KW - RESISTANCE

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ER -

Multi trace element profiling in pathogenic and non-pathogenic fungi

Abstract

Bibliographical note

Keywords

UN SDGs

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