Comparative genomic analysis of thermophilic fungi reveals convergent evolutionary adaptations and gene losses

Andrei S Steindorff; Maria Victoria Aguilar-Pontes; Aaron J Robinson; Bill Andreopoulos; Kurt LaButti; Alan Kuo; Stephen Mondo; Robert Riley; Robert Otillar; Sajeet Haridas; Anna Lipzen; Jane Grimwood; Jeremy Schmutz; Alicia Clum; Ian D Reid; Marie-Claude Moisan; Gregory Butler; Thi Truc Minh Nguyen; Ken Dewar; Gavin Conant; Elodie Drula; Bernard Henrissat; Colleen Hansel; Steven Singer; Miriam I Hutchinson; Ronald P de Vries; Donald O Natvig; Amy J Powell; Adrian Tsang; Igor V Grigoriev

doi:10.1038/s42003-024-06681-w

Comparative genomic analysis of thermophilic fungi reveals convergent evolutionary adaptations and gene losses

Andrei S Steindorff
, Maria Victoria Aguilar-Pontes
, Aaron J Robinson
, Bill Andreopoulos
, Kurt LaButti
, Alan Kuo
, Stephen Mondo
, Robert Riley
, Robert Otillar
, Sajeet Haridas
, Anna Lipzen
, Jane Grimwood
, Jeremy Schmutz
, Alicia Clum
, Ian D Reid
, Marie-Claude Moisan
, Gregory Butler
, Thi Truc Minh Nguyen
, Ken Dewar
, Gavin Conant

Elodie Drula, Bernard Henrissat, Colleen Hansel, Steven Singer, Miriam I Hutchinson, Ronald P de Vries, Donald O Natvig, Amy J Powell, Adrian Tsang, Igor V Grigoriev^*

^*Corresponding author for this work

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

Abstract

Thermophily is a trait scattered across the fungal tree of life, with its highest prevalence within three fungal families (Chaetomiaceae, Thermoascaceae, and Trichocomaceae), as well as some members of the phylum Mucoromycota. We examined 37 thermophilic and thermotolerant species and 42 mesophilic species for this study and identified thermophily as the ancestral state of all three prominent families of thermophilic fungi. Thermophilic fungal genomes were found to encode various thermostable enzymes, including carbohydrate-active enzymes such as endoxylanases, which are useful for many industrial applications. At the same time, the overall gene counts, especially in gene families responsible for microbial defense such as secondary metabolism, are reduced in thermophiles compared to mesophiles. We also found a reduction in the core genome size of thermophiles in both the Chaetomiaceae family and the Eurotiomycetes class. The Gene Ontology terms lost in thermophilic fungi include primary metabolism, transporters, UV response, and O-methyltransferases. Comparative genomics analysis also revealed higher GC content in the third base of codons (GC3) and a lower effective number of codons in fungal thermophiles than in both thermotolerant and mesophilic fungi. Furthermore, using the Support Vector Machine classifier, we identified several Pfam domains capable of discriminating between genomes of thermophiles and mesophiles with 94% accuracy. Using AlphaFold2 to predict protein structures of endoxylanases (GH10), we built a similarity network based on the structures. We found that the number of disulfide bonds appears important for protein structure, and the network clusters based on protein structures correlate with the optimal activity temperature. Thus, comparative genomics offers new insights into the biology, adaptation, and evolutionary history of thermophilic fungi while providing a parts list for bioengineering applications.

Original language	English
Article number	1124
Journal	Communications Biology
Volume	7
Issue number	1
DOIs	https://doi.org/10.1038/s42003-024-06681-w
Publication status	Published - 12 Sept 2024

Bibliographical note

Publisher Copyright:
© Lawrence Berkeley National Laboratory and the Authors 2024.

Funding

The work (proposals: https://doi.org/10.46936/10.25585/60000837 (thermophiles), https://doi.org/10.46936/10.25585/60007442 (Thermoascus aurantiacus), https://doi.org/10.46936/10.25585/60008172 (Acremonium alcalophilum), https://doi.org/10.46936/jejc.proj.2013.48100/60005302 (Acremonium strictum)) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. MVA-P. acknowledges funding by the Maria Zambrano Program from the Spanish Ministry of Science and Innovation (MICINN) for the attraction of international talent and grant PID2022-140187OB-I00 and by an UCOLIDERA grant from the University of C\u00F3rdoba. AT acknowledges funding by Genome Canada and Genome Quebec for the support of the sequencing, assembly and annotation of the CSFG genomes.

Funders	Funder number
U.S. Department of Energy Joint Genome Institute
Genome Canada
CSFG
Genome Quebec
Universidad de Córdoba
Office of Science
U.S. Department of Energy	DE-AC02-05CH11231
U.S. Department of Energy
Ministerio de Ciencia e Innovación	PID2022-140187OB-I00
Ministerio de Ciencia e Innovación

Keywords

Adaptation, Physiological/genetics
Evolution, Molecular
Fungal Proteins/genetics
Fungi/genetics
Genome, Fungal
Genomics/methods
Phylogeny

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Steindorff, A. S., Aguilar-Pontes, M. V., Robinson, A. J., Andreopoulos, B., LaButti, K., Kuo, A., Mondo, S., Riley, R., Otillar, R., Haridas, S., Lipzen, A., Grimwood, J., Schmutz, J., Clum, A., Reid, I. D., Moisan, M.-C., Butler, G., Nguyen, T. T. M., Dewar, K., ... Grigoriev, I. V. (2024). Comparative genomic analysis of thermophilic fungi reveals convergent evolutionary adaptations and gene losses. Communications Biology, 7(1), Article 1124. https://doi.org/10.1038/s42003-024-06681-w

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title = "Comparative genomic analysis of thermophilic fungi reveals convergent evolutionary adaptations and gene losses",

abstract = "Thermophily is a trait scattered across the fungal tree of life, with its highest prevalence within three fungal families (Chaetomiaceae, Thermoascaceae, and Trichocomaceae), as well as some members of the phylum Mucoromycota. We examined 37 thermophilic and thermotolerant species and 42 mesophilic species for this study and identified thermophily as the ancestral state of all three prominent families of thermophilic fungi. Thermophilic fungal genomes were found to encode various thermostable enzymes, including carbohydrate-active enzymes such as endoxylanases, which are useful for many industrial applications. At the same time, the overall gene counts, especially in gene families responsible for microbial defense such as secondary metabolism, are reduced in thermophiles compared to mesophiles. We also found a reduction in the core genome size of thermophiles in both the Chaetomiaceae family and the Eurotiomycetes class. The Gene Ontology terms lost in thermophilic fungi include primary metabolism, transporters, UV response, and O-methyltransferases. Comparative genomics analysis also revealed higher GC content in the third base of codons (GC3) and a lower effective number of codons in fungal thermophiles than in both thermotolerant and mesophilic fungi. Furthermore, using the Support Vector Machine classifier, we identified several Pfam domains capable of discriminating between genomes of thermophiles and mesophiles with 94\% accuracy. Using AlphaFold2 to predict protein structures of endoxylanases (GH10), we built a similarity network based on the structures. We found that the number of disulfide bonds appears important for protein structure, and the network clusters based on protein structures correlate with the optimal activity temperature. Thus, comparative genomics offers new insights into the biology, adaptation, and evolutionary history of thermophilic fungi while providing a parts list for bioengineering applications.",

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author = "Steindorff, \{Andrei S\} and Aguilar-Pontes, \{Maria Victoria\} and Robinson, \{Aaron J\} and Bill Andreopoulos and Kurt LaButti and Alan Kuo and Stephen Mondo and Robert Riley and Robert Otillar and Sajeet Haridas and Anna Lipzen and Jane Grimwood and Jeremy Schmutz and Alicia Clum and Reid, \{Ian D\} and Marie-Claude Moisan and Gregory Butler and Nguyen, \{Thi Truc Minh\} and Ken Dewar and Gavin Conant and Elodie Drula and Bernard Henrissat and Colleen Hansel and Steven Singer and Hutchinson, \{Miriam I\} and \{de Vries\}, \{Ronald P\} and Natvig, \{Donald O\} and Powell, \{Amy J\} and Adrian Tsang and Grigoriev, \{Igor V\}",

note = "Publisher Copyright: {\textcopyright} Lawrence Berkeley National Laboratory and the Authors 2024.",

year = "2024",

month = sep,

day = "12",

doi = "10.1038/s42003-024-06681-w",

language = "English",

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Steindorff, AS, Aguilar-Pontes, MV, Robinson, AJ, Andreopoulos, B, LaButti, K, Kuo, A, Mondo, S, Riley, R, Otillar, R, Haridas, S, Lipzen, A, Grimwood, J, Schmutz, J, Clum, A, Reid, ID, Moisan, M-C, Butler, G, Nguyen, TTM, Dewar, K, Conant, G, Drula, E, Henrissat, B, Hansel, C, Singer, S, Hutchinson, MI, de Vries, RP, Natvig, DO, Powell, AJ, Tsang, A & Grigoriev, IV 2024, 'Comparative genomic analysis of thermophilic fungi reveals convergent evolutionary adaptations and gene losses', Communications Biology, vol. 7, no. 1, 1124. https://doi.org/10.1038/s42003-024-06681-w

TY - JOUR

T1 - Comparative genomic analysis of thermophilic fungi reveals convergent evolutionary adaptations and gene losses

AU - Steindorff, Andrei S

AU - Aguilar-Pontes, Maria Victoria

AU - Robinson, Aaron J

AU - Andreopoulos, Bill

AU - LaButti, Kurt

AU - Kuo, Alan

AU - Mondo, Stephen

AU - Riley, Robert

AU - Otillar, Robert

AU - Haridas, Sajeet

AU - Lipzen, Anna

AU - Grimwood, Jane

AU - Schmutz, Jeremy

AU - Clum, Alicia

AU - Reid, Ian D

AU - Moisan, Marie-Claude

AU - Butler, Gregory

AU - Nguyen, Thi Truc Minh

AU - Dewar, Ken

AU - Conant, Gavin

AU - Drula, Elodie

AU - Henrissat, Bernard

AU - Hansel, Colleen

AU - Singer, Steven

AU - Hutchinson, Miriam I

AU - de Vries, Ronald P

AU - Natvig, Donald O

AU - Powell, Amy J

AU - Tsang, Adrian

AU - Grigoriev, Igor V

PY - 2024/9/12

Y1 - 2024/9/12

N2 - Thermophily is a trait scattered across the fungal tree of life, with its highest prevalence within three fungal families (Chaetomiaceae, Thermoascaceae, and Trichocomaceae), as well as some members of the phylum Mucoromycota. We examined 37 thermophilic and thermotolerant species and 42 mesophilic species for this study and identified thermophily as the ancestral state of all three prominent families of thermophilic fungi. Thermophilic fungal genomes were found to encode various thermostable enzymes, including carbohydrate-active enzymes such as endoxylanases, which are useful for many industrial applications. At the same time, the overall gene counts, especially in gene families responsible for microbial defense such as secondary metabolism, are reduced in thermophiles compared to mesophiles. We also found a reduction in the core genome size of thermophiles in both the Chaetomiaceae family and the Eurotiomycetes class. The Gene Ontology terms lost in thermophilic fungi include primary metabolism, transporters, UV response, and O-methyltransferases. Comparative genomics analysis also revealed higher GC content in the third base of codons (GC3) and a lower effective number of codons in fungal thermophiles than in both thermotolerant and mesophilic fungi. Furthermore, using the Support Vector Machine classifier, we identified several Pfam domains capable of discriminating between genomes of thermophiles and mesophiles with 94% accuracy. Using AlphaFold2 to predict protein structures of endoxylanases (GH10), we built a similarity network based on the structures. We found that the number of disulfide bonds appears important for protein structure, and the network clusters based on protein structures correlate with the optimal activity temperature. Thus, comparative genomics offers new insights into the biology, adaptation, and evolutionary history of thermophilic fungi while providing a parts list for bioengineering applications.

AB - Thermophily is a trait scattered across the fungal tree of life, with its highest prevalence within three fungal families (Chaetomiaceae, Thermoascaceae, and Trichocomaceae), as well as some members of the phylum Mucoromycota. We examined 37 thermophilic and thermotolerant species and 42 mesophilic species for this study and identified thermophily as the ancestral state of all three prominent families of thermophilic fungi. Thermophilic fungal genomes were found to encode various thermostable enzymes, including carbohydrate-active enzymes such as endoxylanases, which are useful for many industrial applications. At the same time, the overall gene counts, especially in gene families responsible for microbial defense such as secondary metabolism, are reduced in thermophiles compared to mesophiles. We also found a reduction in the core genome size of thermophiles in both the Chaetomiaceae family and the Eurotiomycetes class. The Gene Ontology terms lost in thermophilic fungi include primary metabolism, transporters, UV response, and O-methyltransferases. Comparative genomics analysis also revealed higher GC content in the third base of codons (GC3) and a lower effective number of codons in fungal thermophiles than in both thermotolerant and mesophilic fungi. Furthermore, using the Support Vector Machine classifier, we identified several Pfam domains capable of discriminating between genomes of thermophiles and mesophiles with 94% accuracy. Using AlphaFold2 to predict protein structures of endoxylanases (GH10), we built a similarity network based on the structures. We found that the number of disulfide bonds appears important for protein structure, and the network clusters based on protein structures correlate with the optimal activity temperature. Thus, comparative genomics offers new insights into the biology, adaptation, and evolutionary history of thermophilic fungi while providing a parts list for bioengineering applications.

KW - Adaptation, Physiological/genetics

KW - Evolution, Molecular

KW - Fungal Proteins/genetics

KW - Fungi/genetics

KW - Genome, Fungal

KW - Genomics/methods

KW - Phylogeny

UR - https://www.scopus.com/pages/publications/85203692063

U2 - 10.1038/s42003-024-06681-w

DO - 10.1038/s42003-024-06681-w

M3 - Article

C2 - 39266695

SN - 2399-3642

VL - 7

JO - Communications Biology

JF - Communications Biology

IS - 1

M1 - 1124

ER -

Comparative genomic analysis of thermophilic fungi reveals convergent evolutionary adaptations and gene losses

Abstract

Bibliographical note

Funding

Keywords

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