Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

Ying Chang; Yan Wang; Stephen Mondo; Steven Ahrendt; William Andreopoulos; Kerrie Barry; Jeff Beard; Gerald L Benny; Sabrina Blankenship; Gregory Bonito; Christina Cuomo; Alessandro Desiro; Kyle A Gervers; Hope Hundley; Alan Kuo; Kurt LaButti; B Franz Lang; Anna Lipzen; Kerry O'Donnell; Jasmyn Pangilinan; Nicole Reynolds; Laura Sandor; Matthew E Smith; Adrian Tsang; Igor V Grigoriev; Jason E Stajich; Joseph W Spatafora

doi:10.1016/j.isci.2022.104840

Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

iScience. 2022 Aug 2;25(8):104840. doi: 10.1016/j.isci.2022.104840. eCollection 2022 Aug 19.

Authors

Ying Chang^{1

2}, Yan Wang^{3

4

5}, Stephen Mondo⁶, Steven Ahrendt⁶, William Andreopoulos⁶, Kerrie Barry⁶, Jeff Beard¹, Gerald L Benny⁷, Sabrina Blankenship¹, Gregory Bonito⁸, Christina Cuomo⁹, Alessandro Desiro⁸, Kyle A Gervers¹, Hope Hundley⁶, Alan Kuo⁶, Kurt LaButti⁶, B Franz Lang¹⁰, Anna Lipzen⁶, Kerry O'Donnell¹¹, Jasmyn Pangilinan⁶, Nicole Reynolds⁷, Laura Sandor⁶, Matthew E Smith⁷, Adrian Tsang¹², Igor V Grigoriev^{6

13}, Jason E Stajich³, Joseph W Spatafora¹

Affiliations

¹ Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA.
² Division of Science, Yale-NUS College, Singapore 138527, Singapore.
³ Department of Microbiology and Plant Pathology, Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA 92521, USA.
⁴ Department of Biological Sciences, University of Toronto Scarborough, Toronto, ON M1C 1A4, Canada.
⁵ Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON M5S 3B2, Canada.
⁶ US Department of Energy (DOE) Joint Genome Institute (JGI), Lawrence Berkeley National Lab, Berkeley, CA 94720, USA.
⁷ Department of Plant Pathology, University of Florida, Gainesville, FL 32611, USA.
⁸ Plant Soil and Microbial Sciences, Michigan State University, East Lansing, MI 48824, USA.
⁹ Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge MA 02142, USA.
¹⁰ Robert Cedergren Centre for Bioinformatics and Genomics, Département de Biochimie, Université de Montréal, Montreal, QC, Canada.
¹¹ National Center for Agricultural Utilization Research, US Department of Agriculture, Agricultural Research Service, Peoria, IL 61604, USA.
¹² Centre for Structural and Functional Genomics, Concordia University, Montréal, QC H4B 1R6, Canada.
¹³ Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA.

Abstract

Fungi survive in diverse ecological niches by secreting proteins and other molecules into the environment to acquire food and interact with various biotic and abiotic stressors. Fungal secretome content is, therefore, believed to be tightly linked to fungal ecologies. We sampled 132 genomes from the early-diverging terrestrial fungal lineage zygomycetes (Mucoromycota and Zoopagomycota) and characterized their secretome composition. Our analyses revealed that phylogeny played an important role in shaping the secretome composition of zygomycete fungi with trophic mode contributing a smaller amount. Reconstruction of the evolution of secreted digestive enzymes revealed lineage-specific expansions, indicating that Mucoromycota and Zoopagomycota followed different trajectories early in their evolutionary history. We identified the presence of multiple pathogenicity-related proteins in the lineages known as saprotrophs, suggesting that either the ecologies of these fungi are incompletely known, and/or that these pathogenicity-related proteins have important functions associated with saprotrophic ecologies, both of which invite further investigation.

Keywords: Biological sciences; microbial genomics; microbial metabolism; microbiology; omics.