Comparative genomics reveals multiple causes of variation in mycotoxin production among Fusarium species

Collectively, species of Fusarium produce a diversity of mycotoxins and other secondary metabolites (SMs), but individual species contribute to only a fraction of this diversity. Research over the past two decades has revealed that in Fusarium and other fungi genes responsible for the biosynthesis of an SM are typically clustered. We are using comparative genomic and phylogenetic analyses to investigate the distribution and evolution of SM biosynthetic gene clusters among Fusarium species. These analyses indicate that the distribution of SM clusters differs markedly among species. For example, the fusarubin gene cluster is present in all species of Fusarium examined to date, while the fusarin cluster is widely but not uniformly distributed among species. The trichothecene and fusaric acid clusters have more limited distributions, but their presence is more uniform within the multispecies lineages in which they occur. The fumonisin and zearalenone clusters also exhibit relatively narrow distributions, but their presence within lineages is highly discontinuous (i.e. presence/absence of the clusters can differ among closely related species). In most cases examined, the presence of a biosynthetic gene cluster in a species is the result of vertical inheritance from ancestral species. In some cases, however, the presence of a cluster, and therefore the ability to produce the corresponding SM, is the result of horizontal transfer from another Fusarium species. Cluster loss appears to be the major contributor to discontinuous distribution of gene clusters within lineages of Fusarium. The fumonisin cluster is exemplary of this phenomenon; we have evidence for intact fumonisin cluster homologs in nine fusaria in the F. fujikuroi species complex, but evidence for no cluster or the cluster in various stages of decay in over 40 other members of this complex. Together, variation in the distribution of SM clusters among fusaria, phylogenetic relationships of cluster homologs, and the presence of some cluster homologs in other fungal genera suggest variability in the origins of clusters. Some clusters were likely introduced into Fusarium via vertical inheritance from an ancestor while others were likely introduced via horizontal transfer.