Broad geographical and ecological diversity from similar genomic toolkits in the ascomycete genus Tetracladium

Abstract

The ascomycete genus Tetracladium is best known for containing aquatic hyphomycetes, which are important decomposers in stream food webs. However, some species of Tetracladium are thought to be multifunctional and are also endobionts in plants. Suprisingly, Tetracladium sequences are increasingly being reported from metagenomics and metabarcoding studies of both plants and soils world-wide. It is not clear how these sequences are related to the described species and little is known about the non-aquatic biology of these fungi. Here, the genomes of 24 Tetracladium strains, including all described species, were sequenced and used to resolve relationships among taxa and to improve our understanding of ecological and genomic diversity in this group. All genome-sequenced Tetracladium fungi form a monophyletic group. Conspecific strains of T. furcatum from both aquatic saprotrophic and endobiont lifestyles and a putative cold-adapted clade are identified. Analysis of ITS sequences from water, soil, and plants from around the world reveals that multifunctionality may be widespread through the genus. Further, frequent reports of these fungi from extreme environments suggest they may have important but unknown roles in those ecosystems. Patterns of predicted carbohydrate active enzymes (CAZyme) and secondary metabolites in the Tetracladium genomes are more similar to each other than to other ascomycetes, regardless of ecology, suggesting a strong role for phylogeny shaping genome content in the genus. Tetracladium genomes are enriched for pectate lyase domains (including PL3-2), GH71 -1,3-glucanase domains and CBM24 -1,3-glucan/mutan binding modules, and both GH32 and CBM38, inulinase and inulin binding modules. These results indicate that these fungi are well-suited to digesting pectate and pectin in leaves when living as aquatic hyphomycetes, and inulin when living as root endobionts. Enrichment for -1,3-glucanase domains may be associated with interactions with biofilm forming microorganisms in root and submerged leaf environments.