Horizontal gene transfer in 44 early diverging fungi favors short, metabolic, extracellular proteins from associated bacteria

Abstract

Numerous studies have been devoted to individual cases of horizontally acquired genes in fungi. It has been shown that such genes expand the hosts metabolic capabilities and contribute to their adaptations as parasites or symbionts. Some studies have provided an extensive characterization of the horizontal gene transfer (HGT) in Dikarya. However, in the early diverging fungi (EDF), a similar characterization is still missing. In order to fill this gap, we have designed a computational pipeline to obtain a statistical sample of reliable HGT events with a possibly minimal number of false detections. We have analyzed 44 EDF proteomes and identified 829 xenologs in fungi ranging from Chytridiomycota and Blastocladiomycota to Mucoromycota. We have identified several patterns and statistical properties of EDF HGT. Ancestrally aquatic fungi are generally more likely to acquire foreign genetic material than terrestrial ones. Endosymbiotic bacteria can be a source of useful xenologs, as exemplified by NOD-like receptors transferred to Mortierellomycota. Closely related fungi have similar rates of intronization of xenologs. The number of post-transfer paralogs of a protein can be described by a heavy-tailed Yule-Simons distribution. Post-transfer gene fusions complicate the landscape of HGT. We have designed a methodology to obtain a reliable, statistical sample of inter-kingdom xenologs across the tree of life of EDF to give a preliminary characterization of their general properties and patterns. We show that HGT is driven by bursts of gene exchange and duplication, resulting in highly divergent numbers and molecular properties of xenologs between fungal lineages. A close ecological relationship with another organism seems to be a predisposing condition for HGT, but does not always result in an extensive gene exchange. We argue that there is no universal approach for HGT identification and inter- and intra kingdom transfers require tailored identification methods. Our results help to better understand how and to what extent HGT has shaped the metabolic, adaptive, and immune capabilities of fungi.