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

Journal Article · · Communications Biology
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  1. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
  2. Concordia University, Montreal, QC (Canada); University of Córdoba (Spain)
  3. Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
  4. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
  5. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  6. Concordia University, Montreal, QC (Canada)
  7. McGill Univ., Montreal, QC (Canada)
  8. North Carolina State University, Raleigh, NC (United States)
  9. Aix Marseille Univ. (France); Centre National de la Recherche Scientifique (CNRS) (France)
  10. Technical Univ. of Denmark, Lyngby (Denmark)
  11. Woods Hole Oceanographic Institution, Woods Hole, MA (United States)
  12. Joint BioEnergy Institute (JBEI), Emeryville, CA (United States)
  13. Univ. of New Mexico, Albuquerque, NM (United States)
  14. Utrecht University (Netherlands)
  15. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
  16. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); University of California, Berkeley, CA (United States)
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.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2447197
Alternate ID(s):
OSTI ID: 2499466
Journal Information:
Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 7; ISSN 2399-3642
Publisher:
Springer NatureCopyright Statement
Country of Publication:
United States
Language:
English

References (41)

ABC‐F translation factors: from antibiotic resistance to immune response journal December 2020
Predicting Secretory Proteins with SignalP book January 2017
The ‘effective number of codons’ used in a gene journal March 1990
Enzymes and enzymatic mechanisms in enzymatic degradation of lignocellulosic biomass: A mini-review journal January 2023
The SDR (short-chain dehydrogenase/reductase and related enzymes) nomenclature initiative journal March 2009
A molecular phylogeny of thermophilic fungi journal April 2012
101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens journal June 2020
Genome-scale phylogeny and comparative genomics of the fungal order Sordariales journal December 2023
Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism journal September 2008
Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris journal October 2011
Identification of a deep-branching thermophilic clade sheds light on early bacterial evolution journal July 2023
Ecological selection for small microbial genomes along a temperate-to-thermal soil gradient journal November 2018
Highly accurate protein structure prediction with AlphaFold journal July 2021
Fast and accurate protein structure search with Foldseek journal May 2023
ColabFold: making protein folding accessible to all journal May 2022
Small genome of the fungus Escovopsis weberi , a specialized disease agent of ant agriculture journal March 2016
CAFE: a computational tool for the study of gene family evolution journal March 2006
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
The MaSuRCA genome assembler journal August 2013
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs journal June 2015
mycoCLAP, the database for characterized lignocellulose-active proteins of fungal origin: resource and text mining curation support journal January 2015
Causes and Consequences of Genome Expansion in Fungi journal November 2011
Growth Temperature and Genome Size in Bacteria Are Negatively Correlated, Suggesting Genomic Streamlining During Thermal Adaptation journal April 2013
Kingdom-Wide Analysis of Fungal Protein-Coding and tRNA Genes Reveals Conserved Patterns of Adaptive Evolution journal January 2022
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
TimeTree: A Resource for Timelines, Timetrees, and Divergence Times journal April 2017
Phosphoesterase domains associated with DNA polymerases of diverse origins journal August 1998
The worldwide Protein Data Bank (wwPDB): ensuring a single, uniform archive of PDB data journal January 2007
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
Heat shock response of thermophilic fungi: membrane lipids and soluble carbohydrates under elevated temperatures journal June 2016
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Novel β-structure of YLR301w fromSaccharomyces cerevisiae journal April 2012
Diversity of genomic adaptations to the post‐fire environment in Pezizales fungi points to crosstalk between charcoal tolerance and sexual development journal September 2022
Thermophilic Fungi: Their Physiology and Enzymes journal September 2000
Heat shock response in the thermophilic fungus Rhizomucor miehei journal September 2014
SnowyOwl: accurate prediction of fungal genes by using RNA-Seq and homology information to select among ab initio models journal July 2014
SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler journal December 2012
OrthoFinder: phylogenetic orthology inference for comparative genomics journal November 2019
Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement journal November 2014

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