The interkingdom horizontal gene transfer in 44 early diverging fungi is driven by bursts of gene exchange and duplication, resulting in boosted adaptive capabilities of selected lineages

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 genomes and identified 185 phylogenetic trees with 1077 xenologs 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. A close ecological relationship with another organism is a predisposing condition for HGT, as exemplified by a transfer of NOD-like receptors between Mortierellomycotina and their symbiotic bacteria, but does not always result in an extensive gene exchange. Closely related fungi have similar rates of intronization of xenologs. The evolution of the number of xenologs after transfer can be explained by the Yule model of speciation. Post-transfer gene fusions complicate the landscape of HGT. Importance Although it is now recognized that horizontal gene exchange is a factor influencing the adaptation and evolution of eukaryotic organisms, the so far described cases in early diverging fungi (EDF) are fragmentary, and a large-scale comprehensive study is lacking. 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 study how different fungal lineages vary in terms of the number of xenologs, what are their ecological associations, and the molecular properties of proteins encoded by the acquired genes. Our results help to better understand to what extent and in what way the incorporation of foreign genetic material shaped the metabolic, adaptive, and immune capabilities of fungi.