Distribution and shared evolutionary history of the Fumonisin and AAL toxin biosynthetic gene clusters

Background: Fumonisins are among the mycotoxins of most concern to food safety and are structurally similar to AAL toxins, a family of host selective toxins. Together, these two toxin families are produced by ecologically diverse species in three fungal classes: AAL toxins by Alternaria arborescens in class Dothideomycetes and fumonisins by Aspergillus species in class Eurotiomycetes and by Fusarium and Tolypocladium species in class Sordariomycetes. Although structural similarities suggest that AAL toxins and fumonisins have a common biogenic origin, the evolutionary origins and relationships of their biosynthetic genes are not clear. Results: Here, we used BLAST, comparative genomic, phylogenetic, and functional analyses to identify and characterize homologs of the fumonisin biosynthetic gene (FUM) cluster in fungi. Our analyses identified FUM cluster homologs in A. arborescens and in species of Aspergillus, Bipolaris, Fusarium, and Tolypocladium. The results also suggest that the FUM cluster likely evolved from an ancestral cluster with 11 FUM genes through multiple mechanisms, including (1) vertical transmission, (2) acquisition of additional genes by some cluster lineages, (3) duplication of individual FUM genes, and (4) either horizontal transfer of the cluster from the Sordariomycetes to the Dothideomycetes or duplication and differential loss. Overall, our results suggest that the AAL toxin and FUM clusters share a common evolutionary origin and indicate that structural variation of the chemical products of AAL toxins and fumonisins has resulted from variation in FUM gene content and function. Conclusions: The presence of FUM clusters in relatively few classes of fungi with distinct lifestyles (plant versus insect/animal pathogens) suggests an important role of FUM metabolites in diverse fungal-host interactions. This study advances our understanding of the role of specific FUM genes in toxin biosynthesis and will improve our ability to detect and predict the ability of fungi found in food and animal feed to synthesize these mycotoxins.