Cited by 79Yeasts and Rust Fungi StudiesFungal and yeast genetics researchAntifungal resistance and susceptibility

Distribution and impact of yeast thermal tolerance permissive for mammalian infection

Open access
Robert, Vincent, Cardinali, Gianluigi, Casadevall, Arturo·2015·BMC Biology

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s12915-015-0127-3

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 43 · Cited by 79

Research works printed but not linked: 40

  1. [1]Maheshwari R Bharadwaj G Bhat MK Thermophilic fungi: their physiology and enzymes Microbiol Mol Biol Rev. 2000 64 461 88 10.1128/MMBR.64.3.461-488.2000 10974122 PMC99000 · DOI
  2. [2]Tansey MR Brock TD The upper temperature limit for eukaryotic organisms Proc Natl Acad Sci U S A. 1972 69 2426 8 10.1073/pnas.69.9.2426 4506763 PMC426956 · DOI
  3. [3]Blehert DS Hicks AC Behr M Meteyer CU Berlowski-Zier BM Buckles EL Bat white-nose syndrome: an emerging fungal pathogen? Science. 2009 323 227 10.1126/science.1163874 18974316 · DOI
  4. [4]Meteyer CU Valent M Kashmer J Buckles EL Lorch JM Blehert DS Recovery of little brown bats (Myotis lucifugus) from natural infection with Geomyces destructans, white-nose syndrome J Wildl Dis. 2011 47 618 26 10.7589/0090-3558-47.3.618 21719826 · DOI
  5. [5]Rowley JJ Alford RA Hot bodies protect amphibians against chytrid infection in nature Sci Rep. 2013 3 1515 10.1038/srep01515 23519020 PMC3604863 · DOI
  6. [6]Woodhams DC Alford RA Marantelli G Emerging disease of amphibians cured by elevated body temperature Dis Aquat Organ. 2003 55 65 7 10.3354/dao055065 12887256 · DOI
  7. [7]Heard GW Scroggie MP Clemann N Ramsey DS Wetland characteristics influence disease risk for a threatened amphibian Ecol Appl. 2014 24 650 62 10.1890/13-0389.1 24988766 · DOI
  8. [8]Robert VA Casadevall A Vertebrate endothermy restricts most fungi as potential pathogens J Infect Dis. 2009 200 1623 6 10.1086/644642 19827944 · DOI
  9. [9]Perfect JR Lang SDR Durack DT Chronic cryptococcal meningitis Am J Path. 1980 101 177 93 7004196 PMC1903580
  10. [10]Bergman F Effect of temperature on intratesticular cryptococcal infection in rabbits Sabouraudia. 1966 5 54 8 10.1080/00362176785190101 5963262 · DOI
  11. [11]Garcia-Solache MA Izquierdo-Garcia D Smith C Bergman A Casadevall A Fungal virulence in a lepidopteran model is an emergent property with deterministic features mBio. 2013 4 e00100 13 10.1128/mBio.00100-13 23631914 PMC3648900 · DOI
  12. [12]Bergman A Casadevall A Mammalian endothermy optimally restricts fungi and metabolic costs MBio. 2010 1 e00212 10 10.1128/mBio.00212-10 21060737 PMC2975364 · DOI
  13. [13]Casadevall A Fungal virulence, vertebrate endothermy, and dinosaur extinction: is there a connection? Fungal Genet Biol. 2005 42 98 106 10.1016/j.fgb.2004.11.008 15670708 · DOI
  14. [14]Casadevall A Fungi and the rise of mammals PLoS Pathog. 2012 8 e1002808 10.1371/journal.ppat.1002808 22916007 PMC3420938 · DOI
  15. [16]Garcia-Solache MA Casadevall A Global warming will bring new fungal diseases for mammals MBio. 2010 1 e00100 13 10.1128/mBio.00061-10 PMC2912667 20689745 · DOI
  16. [17]De CE Jaronski S Lyons B Lyons TJ Keyhani NO Directed evolution of a filamentous fungus for thermotolerance BMC Biotechnol. 2009 9 74 10.1186/1472-6750-9-74 19709419 PMC2741439 · DOI
  17. [18]Harris JR Lockhart SR Sondermeyer G Vugia DJ Crist MB D’Angelo MT Cryptococcus gattii infections in multiple states outside the US Pacific Northwest Emerg Infect Dis. 2013 19 1620 6 24050410 PMC3810751
  18. [19]Patel A Hammersmith K Contact lens-related microbial keratitis: recent outbreaks Curr Opin Ophthalmol. 2008 19 302 6 10.1097/ICU.0b013e3283045e74 18545011 · DOI
  19. [20]Casadevall A Pirofski LA Exserohilum rostratum fungal meningitis associated with methylprednisolone injections Future Microbiol. 2013 8 135 7 10.2217/fmb.12.138 23374119 PMC3969233 · DOI
  20. [22]Bowman BH White TJ Taylor JW Human pathogenic fungi and their close nonpathogenic relatives Mol Phylogenet Evol. 1996 6 89 96 10.1006/mpev.1996.0061 8812309 · DOI
  21. [23]Legendre P Legendre L Unweighted Pair Group Method with Arithmetic Mean is a simple and very common agglomerative hierarchical clustering method Numerica Ecology. Second English Edition. Developments in Environmental Modeling 20 1998 Amsterdam Elsevier
  22. [24]Cabanes FJ Malassezia yeasts: how many species infect humans and animals? PLoS Pathog. 2014 10 e1003892 10.1371/journal.ppat.1003892 24586146 PMC3937305 · DOI
  23. [26]Van Der Walt JP Hopsu-Havu VK A colour reaction for the differentiation of ascomycetous and hemibasidiomycetous yeasts Antonie Van Leeuwenhoek. 1976 42 157 63 10.1007/BF00399460 60081 · DOI
  24. [27]van Maris AJ Bakker BM Brandt M Boorsma A de Mattos MJT Grivell LA Modulating the distribution of fluxes among respiration and fermentation by overexpression of HAP4 in Saccharomyces cerevisiae FEMS Yeast Res. 2001 1 139 49 10.1111/j.1567-1364.2001.tb00025.x 12702359 · DOI
  25. [28]Cardinali G Vollenbroich V Jeon MS de Graaf AA Hollenberg CP Constitutive expression in gal7 mutants of Kluyveromyces lactis is due to internal production of galactose as an inducer of the Gal/Lac regulon Mol Cell Biol. 1997 17 1722 30 9032299 PMC231897
  26. [31]Desnos-Ollivier M Robert V Raoux-Barbot D Groenewald M Dromer F Antifungal susceptibility profiles of 1698 yeast reference strains revealing potential emerging human pathogens PLoS One. 2012 7 e32278 10.1371/journal.pone.0032278 22396754 PMC3291558 · DOI
  27. [32]Liu Z Pagani M Zinniker D Deconto R Huber M Brinkhuis H Global cooling during the eocene-oligocene climate transition Science. 2009 323 1187 90 10.1126/science.1166368 19251622 · DOI
  28. [33]Siccardi D Rellini P Corte L Bistoni F Fatichenti F Cardinali G General evidence supporting the hypothesis that Saccharomyces cerevisiae vaginal isolates originate from food industrial environments New Microbiol. 2006 29 201 6 17058787
  29. [34]Brown GD Denning DW Gow NA Levitz SM Netea MG White TC Hidden killers: human fungal infections Sci Transl Med 2012 4 165rv13 10.1126/scitranslmed.3004404 23253612 · DOI · Paper page
  30. [35]Casadevall A Amoeba provide insight into the origin of virulence in pathogenic fungi Adv Exp Med Biol. 2012 710 1 10 10.1007/978-1-4419-5638-5_1 22127880 · DOI
  31. [36]Fraser JA Giles SS Wenink EC Geunes-Boyer SG Wright JR Diezmann S Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak Nature. 2005 437 1360 4 10.1038/nature04220 16222245 · DOI · Paper page
  32. [37]Casadevall A Pirofski L The damage-response framework of microbial pathogenesis Nature Microbiol Rev. 2003 1 17 24 10.1038/nrmicro732 PMC7097162 15040176 · DOI
  33. [38]Storck R Nucleotide composition of nucleic acids of fungi. II. Deoxyribonucleic acids J Bacteriol. 1966 91 227 30 5948191 PMC315936
  34. [39]Xu Y Wang Y Yan L Liang RM Dai BD Tang RJ Proteomic analysis reveals a synergistic mechanism of fluconazole and berberine against fluconazole-resistant Candida albicans: endogenous ROS augmentation J Proteome Res. 2009 8 5296 304 10.1021/pr9005074 19754040 · DOI · Paper page
  35. [40]Calahorra M Sanchez NS Pena A Characterization of glycolytic metabolism and ion transport of Candida albicans Yeast. 2012 29 357 70 10.1002/yea.2915 22899221 · DOI
  36. [41]Rozpedowska E Galafassi S Johansson L Hagman A Piskur J Compagno C Candida albicans–a pre-whole genome duplication yeast–is predominantly aerobic and a poor ethanol producer FEMS Yeast Res. 2011 11 285 91 10.1111/j.1567-1364.2010.00715.x 21205163 · DOI
  37. [42]Hall RA De SL Maccallum DM Topal H Eaton R Bloor JW CO(2) acts as a signalling molecule in populations of the fungal pathogen Candida albicans PLoS Pathog. 2010 6 e1001193 10.1371/journal.ppat.1001193 21124988 PMC2987819 · DOI · Paper page
  38. [43]Zhao C Jung US Garrett-Engele P Roe T Cyert MS Levin DE Temperature-induced expression of yeast FKS2 is under the dual control of protein kinase C and calcineurin Mol Cell Biol. 1998 18 1013 22 9447998 PMC108813
  39. [44]Maligie MA Selitrennikoff CP Cryptococcus neoformans resistance to echinocandins: (1,3)beta-glucan synthase activity is sensitive to echinocandins Antimicrob Agents Chemother. 2005 49 2851 6 10.1128/AAC.49.7.2851-2856.2005 15980360 PMC1168702 · DOI · Paper page
  40. [45]Feldmesser M Kress Y Mednick A Casadevall A The effect of the echinocandin analogue caspofungin on cell wall glucan synthesis by Cryptococcus neoformans J Infect Dis. 2000 182 1791 5 10.1086/317614 11069257 · DOI

Authors
Robert, V., Cardinali, G., & Casadevall, A.
Affiliations
  • Westerdijk Fungal Biodiversity Institute (NL)
  • University of Perugia (IT)
  • Albert Einstein College of Medicine (US)
Corresponding author
  • Robert, Vincent
  • Cardinali, Gianluigi
  • Casadevall, Arturo
Venue
BMC Biology
Published
2015-02-26
Volume
13
Issue
1
Pages
18-18
ISSN
1741-7007 (ISSN-L)
OpenAlex
W2075455725
Cited by
79
References
43
Citations by year
2026: 6 · 2025: 16 · 2024: 9 · 2023: 9 · 2022: 8 · 2021: 8 · 2020: 7 · 2019: 8 · 2018: 4 · 2017: 2 · 2016: 2
FWCI
1.16
Type
journal article
Language
en
Open access
Locations
  • BMC Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
  • National Institutes of Health (5r01hl059842-23, 5r01ai052733-16, 5R01AI052733, 5R37AI033142, 5R01HL059842, 5r37ai033142-24)
  • National Heart, Lung, and Blood Institute (R01-HL059842, 5R01HL059842)
  • National Institute of Allergy and Infectious Diseases (R37-AI033142, R01-AI052733, 5R37AI033142, 5R01AI052733., R01AI033774)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Keywords
fungal virulence, mammalian infection, ascomycetous yeasts, basidiomycetous yeasts, antifungal resistance, fermentative capacity, carbon source assimilation, latitude, climate change adaptation
MeSH terms
Adaptation, Physiological, Animals, Antifungal Agents, Fermentation, Geography, Glucose, Humans, Mammals, Microbial Sensitivity Tests, Mycoses, Phylogeny, Temperature, Yeasts, Genetic Loci

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review