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

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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Journal
Communications Biology
Published
2024-09-12
DOI
https://doi.org/10.1038/s42003-024-06681-w
Citations
21
Primary Topic
Genomics and Phylogenetic Studies
Type
article
Field-Weighted Citation Impact
4.91

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

Miriam I. Hutchinson, Igor V. Grigoriev, Stephen J. Mondo, Andrei Stecca Steindorff et al.
21 citations
Communications Biology
Genomics and Phylogenetic Studies
4.91
article

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

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

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.

Communications BiologyVol. 7(1)
Centre National de la Recherche Scientifique (FR), Los Alamos National Laboratory (US), North Carolina State University (US), Lawrence Berkeley National Laboratory (US), University of New Mexico (US), Sandia National Laboratories California (US), Utrecht University (NL), Joint Genome Institute (US), Aix-Marseille Université (FR), Sandia National Laboratories (US), Biodiversité et Biotechnologie Fongiques (FR), Westerdijk Fungal Biodiversity Institute (NL), HudsonAlpha Institute for Biotechnology (US), Architecture et Fonction des Macromolécules Biologiques (FR), McGill University (CA), Joint BioEnergy Institute (US), University of Córdoba (ES), Concordia University (CA), Woods Hole Oceanographic Institution (US), University of California, Berkeley (US), Technical University of Denmark (DK)
U.S. Department of Energy, Genome Canada, Joint Genome Institute, Ministerio de Ciencia e Innovación, Universidad de Córdoba, Office of Science
Peace, Justice and strong institutions
Openalex Percentile: Top 4%
Genomics and Phylogenetic Studies
4.91
DOIOpen Access PDFOpenAlex
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