Fusarium abutilonis and F. guadeloupense, two novel species in the Fusarium buharicum clade supported by multilocus molecular phylogenetic analyses

Authors: O Donnell, Kerry; GRAFENHAN, TOM - Agriculture And Agri-Food Canada; LARABA, IMANE - Orise Fellow; Busman, Mark; Proctor, Robert; Kim, Hye-Seon; WIEDERHOLD, NATHAN - University Of Texas Health Science Center; GEISER, DAVID - Pennsylvania State University; SEIFERT, KEITH - Carleton University - Canada

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/26/2022
Publication Date: 6/9/2022
Citation: O'Donnell, K., Grafenhan, T., Laraba, I., Busman, M., Proctor, R.H., Kim, H.-S., Wiederhold, N.P., Geiser, D.M., Seifert, K.A. 2022. Fusarium abutilonis and F. guadeloupense, two novel species in the Fusarium buharicum clade supported by multilocus molecular phylogenetic analyses. Mycologia. 114(4):682-696. https://doi.org/10.1080/00275514.2022.2071563.
DOI: https://doi.org/10.1080/00275514.2022.2071563

Interpretive Summary: Fusarium diseases and their toxins are responsible for multibillion U.S. dollar losses to the world’s agricultural economy. Ongoing genetic analyses of fusaria housed in the Agricultural Research Service Culture Collection (NRRL; https://nrrl.ncaur.usda.gov/) indicate that this agronomically important genus comprises over 450 species. Given the omnipresent threat that these pathogens and their diverse toxins pose to global agricultural biosecurity, food safety and human health, detailed DNA-based studies published over the past quarter century have focused on the largest and most important mycotoxin-producing and phytopathogenic lineages. However, no detailed molecular genetic analyses of the F. buharicum species complex has been conducted to date. Therefore, the present study was initiated to investigate pathogen diversity within this complex and assess their potential to produce toxins on cracked maize kernel cultures and from analyses of whole genome sequence data. The comparative genomic analyses revealed that these fungi possess the genetic machinery to produce five different toxins (i.e., fumonisins, trichothecenes, fusaric acid, bikaverin and equisetin) of concern to food and feed safety. However, only equisetin toxin was detected in the cracked maize kernel cultures. Therefore, additional studies are needed to identify the optimal conditions under which all five toxins are produced to more critically assess the threat these molds pose to food safety and human health.

Technical Abstract: This study was conducted to elucidate evolutionary relationships and species diversity within the Fusarium buharicum species complex (FBSC). We also evaluate the potential of these species to produce mycotoxins and other bioactive secondary metabolites. Maximum likelihood and maximum parsimony analyses of aligned DNA sequences from portions of four marker loci (ITS rDNA, TEF1, RPB1, and RPB2) and the combined 4495 bp dataset support recognition of seven genealogically exclusive species within the FBSC. Two of the three newly discovered species are formally described as F. abutilonis and F. guadeloupense based on concordance of gene genealogies and morphological data. Fusarium abutilonis induces leaf, stem and root lesions on several weedy Malvaceae (Abution theophrasti, Anoda cristata, Sida spinosa) and a fabaceous host (Senna obtusifolia) in North America and also was recovered from soil in New Caledonia. Fusarium abutilonis, together with its unnamed sister, Fusarium sp. ex marshmallow (Hibiscus moscheutos) from Washington State, and F. buharicum pathogenic to cotton and kenaf in Russia and Iran, respectively, were strongly supported as a clade of malvaceous pathogens. The four other species of the FBSC are not known to be phytopathogenic; however, F. guadeloupense was isolated from human blood in Texas and soil in Guadeloupe. The latter isolate is unique because it represents the only known case of a fusarial infection disseminated hematogenously by a species lacking microconidia and the only documented fusariosis caused by a member of the FBSC. Whole genome sequence data and extracts of cracked maize kernel cultures were analyzed to assess the potential of FBSC isolates to produce mycotoxins, pigments, and phytohormones.