A yeast love triangle multiple hybridizations shape genome evolution in the Pichia cactophila species complex

Hybrids are chimeric organisms carrying genetic material from at least two divergent parental lineages. Hybridization can contribute to the emergence of novel lineages with unique phenotypic traits that may facilitate their adaptation to new environments. In recent years, genomic analyses have revealed the hybrid nature of several opportunistic human pathogenic yeasts. One of them is Pichia inconspicua, a member of the Pichia cactophila species complex, for which all sequenced strains isolated from Europe are hybrids with so far unknown parentals. It has been recently proposed that P. inconspicua and P. cactophila s.s. should be ranked as the same species due to their genetic similarity. To obtain a better understanding of the evolution of this clade, we sequenced the genomes of the P. cactophila type strain, of its close–relative Pichia pseudocactophila, and of a putative P. inconspicua clinical isolate from Alaska and compared them with the previously sequenced genomes of Pichia norvegensis, P. inconspicua and the recently described Pichia galeolata. Our results show evidence for the existence of distinct lineages with a hybrid origin within this clade and suggest an intricate scenario of recurrent hybridizations in this species complex, some of them giving rise to lineages with the ability to infect humans. Given their different hybridization histories, we propose that P. inconspicua, P. cactophila, and the new clinical isolate from Alaska should represent three distinct species and suggest the name Pichia alaskaensis for the new taxon. Our results clarify the evolutionary relationships within the P. cactophila species complex and underscore the importance of non–vertical evolution.