A novel trichothecene toxin phenotype associated with horizontal gene transfer and a change in gene function in Fusarium

Authors: Proctor, Robert; Hao, Guixia; Kim, Hye-Seon; Whitaker, Briana; LARABA, IMANE - Orise Fellow; Vaughan, Martha; McCormick, Susan

Submitted to: Toxins
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/22/2022
Publication Date: 12/24/2022
Citation: Proctor, R.H., Hao, G., Kim, H.-S., Whitaker, B.K., Laraba, I., Vaughan, M.M., McCormick, S.P. 2022. A novel trichothecene toxin phenotype associated with horizontal gene transfer and a change in gene function in Fusarium. Toxins. 15(1). Article 12. https://doi.org/10.3390/toxins15010012.
DOI: https://doi.org/10.3390/toxins15010012

Interpretive Summary: Some fungi produce toxins that contaminate food and feed crops and are health hazards to humans, pets and livestock. Prior to this study, contamination of crops with one type of toxins known as trichothecenes was attributed to production of the toxins by two groups of species of the fungus Fusarium. We discovered trichothecene production in a new Fusarium species that is distantly related to other trichothecene-producing species. We also found evidence that the ability of the novel species to produce the toxins did not result from the normal process of inheritance—that is, passing of genes from parents to offspring. Instead, the new species gained the ability to produce the toxins by direct transfer of genes from a distantly related species. The results of this study demonstrate that trichothecene toxin production occurs more widely among Fusarium species than was previously known. This study also provided insight into the genetic processes that change both the ability of fungi to produce toxins and the threat fungi pose to human and animal health.

Technical Abstract: Fusarium trichothecenes are among the mycotoxins of most concern to food and feed safety. Production of these mycotoxins and presence of the trichothecene biosynthetic gene (TRI) cluster have been confirmed in only two lineages of Fusarium: the F. sambucinum and Fusarium incarnatum-equiseti species complexes. Here, we identified and characterized a TRI cluster in an undescribed species, Fusarium sp. NRRL 66739, that is reported to be a member of a third Fusarium lineage: the F. buharicum species complex. Cultures of NRRL 66739 accumulated only two trichothecenes, 7-hydroxyisotrichodermin and 7-hydroxyisotrichodermol. Although these are not novel trichothecenes, the production profile of NRRL 66739 is novel, because in previous reports 7-hydroxyisotrichodermin and 7-hydroxyisotrichodermol were components of mixtures of 6 – 8 trichothecenes produced by several Fusarium species in Sambucinum. Heterologous expression analysis indicated that the TRI13 gene in NRRL 66739 confers trichothecene 7-hydroxylation. This contrasts the trichothecene 4-hydroxylation function of TRI13 in other Fusarium species. Phylogenetic analyses suggest that NRRL 66739 acquired the TRI cluster via horizontal gene transfer from a close relative of the F. incarnatum-equiseti and F. sambucinum species complexes. These findings provide insights into evolutionary processes that have shaped the distribution of trichothecene production among Fusarium species and the structural diversity of the toxins.