Distribution and impact of yeast thermal tolerance permissive for mammalian infection

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Abstract

Background

From the viewpoint of fungal virulence in mammals, thermal tolerance can be defined as the ability to grow in the 35°C to 40°C range, which is essential for inhabiting these hosts.

Results

We used archival information in a fungal collection to analyze the relationship between thermal tolerance and genetic background for over 4,289 yeast strains belonging to 1,054 species. Fungal genetic relationships were inferred from hierarchical trees based on pairwise alignments using the rRNA internal transcribed spacer and large subunit rDNA (LSU) sequences. In addition, we searched for correlations between thermal tolerance and other archival information including antifungal susceptibility, carbon sources, and fermentative capacity. Thermal tolerance for growth at mammalian temperatures was not monophyletic, with thermally tolerant species being interspersed among families that include closely related species that are not thermal tolerant. Thermal tolerance and resistance to antifungal drugs were not correlated, suggesting that these two properties evolved independently. Nevertheless, the ability to grow at higher temperatures did correlate with origin from lower geographic latitudes, capacity for fermentation and assimilation of certain carbon sources.

Conclusions

Thermal tolerance was significantly more common among ascomycetous than basidiomycetous yeasts, suggesting an explanation for the preponderance of ascomycetous yeasts among human pathogenic fungi. Analysis of strain maximum tolerable temperature as a function of collection time suggested that basidiomycetous yeasts are rapidly adapting to global warming. The analysis identified genera with a high prevalence of the thermal-tolerant species that could serve as sources of emerging pathogenic fungi.

Electronic supplementary material

The online version of this article (doi:10.1186/s12915-015-0127-3) contains supplementary material, which is available to authorized users.

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Most cited references 35

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Global cooling during the eocene-oligocene climate transition.

Z. Liu, M. Pagani, D. Zinniker … (2009)

About 34 million years ago, Earth's climate shifted from a relatively ice-free world to one with glacial conditions on Antarctica characterized by substantial ice sheets. How Earth's temperature changed during this climate transition remains poorly understood, and evidence for Northern Hemisphere polar ice is controversial. Here, we report proxy records of sea surface temperatures from multiple ocean localities and show that the high-latitude temperature decrease was substantial and heterogeneous. High-latitude (45 degrees to 70 degrees in both hemispheres) temperatures before the climate transition were approximately 20 degrees C and cooled an average of approximately 5 degrees C. Our results, combined with ocean and ice-sheet model simulations and benthic oxygen isotope records, indicate that Northern Hemisphere glaciation was not required to accommodate the magnitude of continental ice growth during this time.

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Vertebrate endothermy restricts most fungi as potential pathogens.

Vincent A. Robert, Arturo Casadevall (2009)

The paucity of fungal diseases in mammals relative to insects, amphibians, and plants is puzzling. We analyzed the thermal tolerance of 4802 fungal strains from 144 genera and found that most cannot grow at mammalian temperatures. Fungi from insects and mammals had greater thermal tolerances than did isolates from soils and plants. Every 1 degrees C increase in the 30 degrees C-40 degrees C range excluded an additional 6% of fungal isolates, implying that fever could significantly increase the thermal exclusion zone. Mammalian endothermy and homeothermy are potent nonspecific defenses against most fungi that could have provided a strong evolutionary survival advantage against fungal diseases.

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Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways.

Beth Fuchs, Eleftherios Mylonakis (2009)

Fungi occupy diverse environments and are subjected to many extreme conditions. Among the stressful conditions faced by fungi are pH changes, osmotic changes, thermal changes, oxide radicals, nutrient deprivation, and exposure to chemicals. These adversities can be found either in the environment or in animal and human hosts. The cell wall integrity (CWI) pathway provides a means to fortify and repair damages to the cell wall in order to withstand stressful environments. The CWI pathway in comprised of cell wall stress sensors that lead to activation of a mitogen-activated protein kinase (MAPK) cascade. Signaling through the MAPK cascade leads to expression of transcription factors that facilitate biosynthesis of cell wall components and actin organization. Given the relatively limited number of components of the CWI pathway and the very diverse stimuli, there must be a means of expanding the pathway. To manage the diverse stress conditions, the CWI pathway cross talks with other pathways or proteins, and these cross talk events enhance the signaling capabilities of the CWI pathway. Lateral influences that facilitate maintaining the cell wall under stress conditions are TOR signaling, calcineurin signaling, the high-osmolarity glycerol pathway, the cyclic AMP-protein kinase A pathway, and additional proteins. In this article, we highlight several of the cross talk events that have been described for Saccharomyces cerevisiae and several other fungi.

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Author and article information

Contributors

Vincent Robert: vrobert@bio-aware.com

Gianluigi Cardinali: gianluigi.cardinali@unipg.it

Arturo Casadevall: arturo.casadevall@einstein.yu.edu

Journal

Journal ID (nlm-ta): BMC Biol

Journal ID (iso-abbrev): BMC Biol

Title: BMC Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1741-7007

Publication date (Electronic): 26 February 2015

Publication date PMC-release: 26 February 2015

Publication date Collection: 2015

Volume: 13

Electronic Location Identifier: 18

Affiliations

[ ]Centraalbureau voor Schimmelcultures CBS, 8 Uppsalalaan, 3584CT Utrecht, The Netherlands

[ ]Department of Pharmaceutical Sciences, University of Perugia, Perugia, Italy

[ ]Department of Microbiology and Immunology and the Division of Infectious Diseases of the Department of Medicine of the Albert Einstein College of Medicine, 1300 Morris Park Ave, Bronx, NY 10461 USA

Article

Publisher ID: 127

DOI: 10.1186/s12915-015-0127-3

PMC ID: 4381509

PubMed ID: 25762372

SO-VID: 3b8e7634-16f3-47d6-bb8e-e61c6e4ad8a6

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 10 December 2014

Date accepted : 10 February 2015

Custom metadata

ScienceOpen disciplines: Life sciences

Keywords: disease,fungi,mammal,taxonomy,temperature

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: disease, fungi, mammal, taxonomy, temperature

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Distribution and impact of yeast thermal tolerance permissive for mammalian infection

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Abstract

Background

Results

Conclusions

Electronic supplementary material

Related collections

Applied use of fungi

Most cited references 35

Global cooling during the eocene-oligocene climate transition.

Vertebrate endothermy restricts most fungi as potential pathogens.

Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways.

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Cited by 30

Most referenced authors 487