A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in Fusarium

Robert H Proctor; Guixia Hao; Hye-Seon Kim; Briana K Whitaker; Imane Laraba; Martha M Vaughan; Susan P McCormick

doi:10.3390/toxins15010012

A Novel Trichothecene Toxin Phenotype Associated with Horizontal Gene Transfer and a Change in Gene Function in Fusarium

Toxins (Basel). 2022 Dec 24;15(1):12. doi: 10.3390/toxins15010012.

Authors

Robert H Proctor¹, Guixia Hao¹, Hye-Seon Kim¹, Briana K Whitaker¹, Imane Laraba², Martha M Vaughan¹, Susan P McCormick¹

Affiliations

¹ Mycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, 1815 N University St., Peoria, IL 61604, USA.
² Oak Ridge Institute for Science and Education, Mycotoxin Prevention and Applied Microbiology, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA.

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 multispecies lineages of Fusarium: the Fusarium incarnatum-equiseti (Incarnatum) and F. sambucinum (Sambucinum) species complexes. Here, we identified and characterized a TRI cluster in a species that has not been formally described and is represented by Fusarium sp. NRRL 66739. This fungus 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 Incarnatum and Sambucinum. 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.

Keywords: Fusarium; biosynthetic gene cluster; horizontal gene transfer; mycotoxin; secondary metabolite; trichothecene.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Fusarium* / metabolism
Gene Transfer, Horizontal
Mycotoxins* / chemistry
Phenotype
Phylogeny
Trichothecenes* / metabolism

Substances

trichothecene
Trichothecenes
Mycotoxins

Supplementary concepts

Fusarium equiseti
Fusarium scirpi

Grants and funding

This work was supported in part by the U.S. Department of Agriculture (USDA), Agricultural Research Service (ARS), Project Number 5010-42000-048-00D. This research was also supported in part by an appointment to the ARS Research Participation Program administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement between the US Department of Energy (DOE) and the USDA. ORISE is managed by ORAU under DOE contract number DE-SC0014664. All opinions expressed in this paper are the author’s and do not necessarily reflect the policies and views of USDA, DOE, or ORAU/ORISE. The mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.