Comparative genomics and phylogenomic investigation of the class Geoglossomycetes provide insights into ecological specialization and the systematics of Pezizomycotina

ABSTRACT

Despite their global presence and ubiquity, members of the class Geoglossomycetes (Pezizomycotina, Ascomycota) are understudied systematically and ecologically. These fungi have long been presumed saprobic due to their occurrence in or near leaf litter and soils. Additionally, they lack an apparent association with other organisms, reinforcing this perception. However, observations of sporocarps near ericaceous shrubs have given rise to an alternative hypothesis that members of Geoglossomycetes may form ericoid mycorrhizae or ectomycorrhizae. This claim, however, has yet to be confirmed via microscopy or amplicon-based studies examining root communities. As a result, our current understanding of their ecology is based on cursory observations. This study presents a comparative analysis of genomic signatures related to ecological niche to investigate the hypothesis of an ericoid mycorrhizal or ectomycorrhizal ecology in the class. We compared the carbohydrate-active enzyme (CAZyme) and secondary metabolite contents of six newly sequenced Geoglossomycetes genomes with those of fungi representing specific ecologies across Pezizomycotina. Our analysis reveals CAZyme and secondary metabolite content patterns consistent with ectomycorrhizal (EcM) members of Pezizomycotina. Specifically, we found a reduction in CAZyme-encoding genes and secondary metabolite clusters that suggests a mutualistic ecology. Our work includes the broadest taxon sampling for a phylogenomic study of Pezizomycotina to date. It represents the first functional genomic and genome-scale phylogenetic study of the class Geoglossomycetes and improves the foundational knowledge of the ecology and evolution of these understudied fungi.

KEYWORDS:

• Ascomycota
• concordance
• gene tree conflict
• Geoglossaceae
• metagenome
• mutualism
• mycorrhizae

Acknowledgments

We thank Alexandra Alexiev, Kevin Amses, Javan K. Carter, Jon Magnuson, Andrew J. Melie, Andrew Monaghan, Angela M. Oliverio, Joseph Spatafora, and Andrew W. Wilson for their contributions to this study; Andrew S. Methven, Vincent P. Hustad, Jean-Marc Moingeon, and C. F. Roobeek for collecting Geoglossomycetes material used in this study; and the BioFrontiers Institute Next-Gen Sequencing Core Facility, which performed the Illumina sequencing and library construction. We also thank two anonymous reviewers for taking the time to read our manuscript thoroughly and provide insightful feedback and suggestions.

Disclosure statement

No potential conflict of interest was reported by the author(s).

DATA AVAILABILITY STATEMENT

Workflows and scripts used to generate these data are publicly available on Tina Melie’s GitHub page: https://github.com/tinamelie/Geoglossomycetes-genomics-workflow. Assembled and annotated genomes were deposited in NCBI GenBank (TABLE S2).

SUPPLEMENTARY MATERIAL

Supplemental data for this article can be accessed online at https://doi.org/10.1080/00275514.2023.2186743

Additional information

Funding

This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under grant [DGE 2040434]. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.Funding for sequencing was provided by Iridian Genomes, grant [IRGEN_RG_2021-1345]: Genomic Studies of Eukaryotic Taxa.This work utilized the Rocky Mountain Advanced Computing Consortuium (RMACC) Summit supercomputer, which is supported by the National Science Foundation [awards ACI-1532235 and ACI-1532236], the University of Colorado Boulder, and Colorado State University. The Summit supercomputer is a joint effort of the University of Colorado Boulder and Colorado State University.