Genomic analysis of Ancylistes closterii, an enigmatic alga parasitic fungus in the arthropod-associated Entomophthoromycotina

Abstract

Recent advances in fungal genome sequencing have dramatically altered our understanding of the phylogeny and evolution of Fungi. However, there are still many poorly studied obligate parasitic or symbiotic fungi for which we lack any genomic information or knowledge of where they fit in the fungal phylogeny. Ancylistes, an endoparasite of desmid green algae, is such an understudied fungal genus. This genus has been taxonomically placed in the group of arthropod pathogens and saprobes, Entomophthoromycotina in Zoopagomycota. Understanding the phylogenetic position of Ancylistes provides insights into the nutritional evolution of Zoopagomycota, which is primarily composed of animal-associated fungi. In this study, we found and cultivated Ancylistes closterii with its host Closterium sp. and sequenced its genome to investigate its phylogenetic position and evolution. Phylogenetic analyses using rDNA and genome-scale datasets showed that A. closterii was sister to other Entomophthoromycotina fungi, confirming the taxonomic position of Ancylistes. Despite the ecological distinctiveness between Ancylistes and other Entomophthoromycotina fungi, our comparative genomic analyses revealed many shared traits of these fungi such as lineage-specific subtilases and hybrid histidine kinases. Ancylistes also possessed unique genes among Zoopagomycota fungi, such as plant cell wall degrading enzymes which could be important for infection of algae. SignificanceImproved taxon sampling is important for inferring a robust phylogeny of Fungi. However, there are still poorly studied obligate parasitic taxa whose DNA sequencing is challenging, especially in Zoopagomycota, one of the early diverging lineages of Fungi. This study focused on a long-neglected algal parasite, Ancylistes closterii, which belongs to the arthropod-associated group, Entomophthoromycotina. We rediscovered A. closterii and established a dual culture of fungus and its host alga, which enabled the first molecular analysis of this enigmatic parasite. Our results provide new insights into the nutritional evolution of primarily animal-associated Zoopagomycota.