Molecular systematics of two sister clades, the Fusarium concolor and F. babinda species complexes, and the discovery of a novel microcycle macroconidium–producing species from South Africa

Authors: JACOBS-VENTER, ADRIANA - Agricultural Research Council Of South Africa; GEISER, DAVID - Pennsylvania State University; LARABA, IMANE - National Higher School Of Agronomy; Busman, Mark; Vaughan, Martha; Proctor, Robert; McCormick, Susan; O Donnell, Kerry

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/18/2018
Publication Date: 12/6/2018
Citation: Jacobs-Venter, A., Laraba, I., Geiser, D.M., Busman, M., Vaughan, M.M., Proctor, R.H., McCormick, S.P., O'Donnell, K. 2018. Molecular systematics of two sister clades, the Fusarium concolor and F. babinda species complexes, and the discovery of a novel microcycle macroconidium–producing species from South Africa. Mycologia. 110:1189-1204. https://doi.org/10.1080/00275514.2018.1526619.
DOI: https://doi.org/10.1080/00275514.2018.1526619

Interpretive Summary: This study was conducted to characterize molds isolated from kikuyu grass associated with a putative mycotoxicosis of cattle in South Africa. This toxicosis is of considerable economic importance because the mortality rate in dairy cows suffering from kikuyu poisoning is high. Symptoms that precede death include gastrointestinal and neuromuscular distress. A putatively novel Fusarium species was isolated from kikuyu grass associated with an outbreak of kikuyu poisoning in 2010 and from plant debris in South African soil. Thus, the present study was initiated to use DNA sequence data from portions of several genes to determine the identity of the isolates recovered from kikuyu grass and to assess their relationship to several closely related species currently stored in the ARS Culture Collection (NRRL) that were received as F. anguioides, F. babinda, F. concolor, and F. polyphialidicum. Genetic analysis of the DNA sequence data indicated that the kiyuyu grass isolates represented a novel species that was formally described as F. austroafricanum. Because this species was implicated in the kikuyu poisoning outbreak, its toxin potential was assessed by analyses of whole-genome sequence data and by toxin analyses of cracked maize kernel cultures. Although analyses of the genome data suggested that F. austroafricanum possessed the genes required to produce at least four different toxins, none were detected in cultures of this mold on cracked corn kernel cultures. Future studies will be directed at determining whether these toxins are produced under different growth conditions. The results of this study should be of interest to toxicologists, veterinarians, and quarantine officials who are charged with developing robust strategies to improve food safety and agricultural biosecurity.

Technical Abstract: Multilocus DNA sequence data were used to investigate species identity and diversity in two sister clades, the Fusarium concolor (FCOSC) and F. babinda species complexes. Of the 109 isolates analyzed, only 4 were received correctly identified to species and these included 1/46 F. concolor, 1/31 F. babinda, and 2/3 F. anguioides. The majority of the F. concolor and F. babinda isolates were received as F. polyphialidicum, which is a heterotypic synonym of the former species. Previously documented from South America, Africa, Europe, and Australia, our data show that F. concolor is also present in North America. The present study expands the known distribution of F. babinda in Australia to Asia, Europe, and North America. The molecular phylogenetic results support the recognition of a novel Fusarium species within the FCOSC, which is described and illustrated here as F. austroafricanum, sp. nov. It was isolated as an endophyte of kikuyu grass associated with a putative mycotoxicosis of cattle and from plant debris in soil in South Africa. Fusarium austroafricanum is most similar morphologically to F. concolor and F. babinda but differs from the latter two species in producing (i) much longer macroconidia in which the apical cell is blunt to slightly papillate and the basal cell is only slightly notched and (ii) macroconidia via microcycle conidiation on water agar. BLASTn searches of the whole genome sequence of F. austroafricanum NRRL 53441 were conducted to predict mycotoxin potential, using genes known to be essential for the synthesis of several mycotoxins and biologically active metabolites. Based on the presence of intact gene clusters that confer the ability to synthesize mycotoxins and pigments, we analyzed cracked corn kernel cultures of F. austroafricanum via liquid chromatography–mass spectrometry (LC-MS) but failed to detect these metabolites in vitro.