Comparative genomics of dark septate endophytes: shedding light on the enigmatic lifestyle and biology of DSEs.

Abstract

Dark septate endophytes (DSE) are widespread root-colonising fungi with poorly understood lifestyle and ecological functions. We investigated their genomic traits, sexual reproduction signatures, carbohydrate-active enzyme (CAZyme) and secondary metabolites profiles, and tested whether genomic features distinguish DSEs and other endophytes from fungi with other lifestyles. We also reconstructed ancestral states to clarify the evolutionary origins of DSEs. We analysed 107 Ascomycota genomes representing diverse lifestyles, including nine newly sequenced DSE genomes. The dataset allowed us to test whether secreted enzyme profiles differ between fungi colonising roots vs shoots and those associated with grass vs nongrass hosts. DSEs evolved through multiple independent trajectories and diverse lifestyles and show remarkable metabolic diversity. They possess extensive degradative capacities and some of the largest biosynthetic gene cluster (BGC) richness among fungi. Despite sharing BGC richness with other endophytes, DSEs form a distinct subgroup with fewer cellulose- and more hemicellulose-targeting enzymes. Genomes also revealed genomic signatures associated with fungi colonising grass vs nongrass hosts and root- vs shoot-associated niches. Our comparative genomics approach highlights how genome-level data can deepen our understanding of endophytic lifestyle and the biology of the enigmatic DSE fungi.