The interkingdom horizontal gene transfer in 44 early diverging fungi boosted their metabolic, adaptive, and immune capabilities

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 low false discovery rate. We have analyzed 44 EDF proteomes and identified 829 xenologs in fungi ranging from Chytridiomycota to Mucoromycota. We have identified several patterns and statistical properties of EDF HGT. 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. 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. Posttransfer gene fusions and losses of protein domains are common and may influence the encoded proteins' functions. 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. Horizontal gene transfer is a transmission of genes between unrelated organisms that seems to occur in all living organisms, including fungi. Although several studies focused on the description of the horizontal gene transfer patterns in terrestrial fungi, similar characterization is still missing for early diverging fungi. Through the development of computational pipeline enabling to obtain a statistical sample of reliable horizontal gene transfer events minimizing false positive hits, we demonstrate that it is driven by bursts of gene exchange and duplication, resulting in highly divergent numbers and molecular properties of xenologs between different fungal lineages. These detected gene transfers seem to expand the metabolic, adaptive, and immune capabilities of early diverging fungi. Horizontal gene transfer is a transmission of genes between organisms, distinct from vertical inheritance from parents to offspring. HGT seems to occur among all living forms. Our study focuses on horizontally transferred genes present in early diverging fungi (EDF). EDF is a relatively understudied group of organisms with vastly diverse lifestyles and tremendous ecological importance. They include arbuscular mycorrhizal Glomeromycota, the gut-dwelling symbionts of herbivores Neocallimastigomycota, or the parasitic Batrachochytrium. HGT has been reported to contribute to this diversity by facilitating niche adaptations in certain lineages. In our work, we have analyzed horizontally acquired genes in 44 fungal genomes, focusing on cases with clear phylogenetic evidence. We have designed a computational pipeline that detects a statistical sample of reliable HGTs. The pipeline is published alongside the article. We have analyzed the donors, acceptors, and properties of the transferred genes. We found transfers of genes that can expand the metabolic, adaptive, and immune capabilities of fungi.