Genome-wide analysis of Fusarium verticillioides reveals inter-kingdom contribution of horizontal gene transfer to the expansion of metabolism

Authors: GAO, SHAN - University Of Georgia; Gold, Scott; WISECAVER, JENNIFER - Purdue University; ZANG, YONG - University Of Massachusetts; GUO, LI - Xian Jiao University; MA, LI-JUN - University Of Massachusetts; ROKAS, ANTONIS - Vanderbilt University; Glenn, Anthony - Tony

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/1/2019
Publication Date: 4/3/2019
Citation: Gao, S., Gold, S.E., Wisecaver, J.H., Zang, Y., Guo, L., Ma, L., Rokas, A., Glenn, A.E. 2019. Genome-wide analysis of Fusarium verticillioides reveals inter-kingdom contribution of horizontal gene transfer to the expansion of metabolism. Fungal Genetics and Biology. 128:60-73. https://doi.org/10.1016/j.fgb.2019.04.002.
DOI: https://doi.org/10.1016/j.fgb.2019.04.002

Interpretive Summary: Horizontal gene transfer (HGT) is the exchange and stable integration of genetic material between unrelated organisms having different evolutionary histories. HGT is rampant in prokaryotes and contributes to observed breaks in species boundaries and generates new biological diversity, including resistance to antibiotics. In eukaryotes HGT is thought to occur at a lower frequency, but with the rapid increase in publicly available genomic data, a growing body of evidence suggests HGT is also a significant factor in the evolution of eukaryotic genomes. Fungi are among the eukaryotic groups where many cases of HGT have been described. The postulated benefits brought to fungi by HGT are the expansion of metabolism, promotion of pathogenicity, and enhanced adaptation to the environment. We hypothesized that the economically important fungus Fusarium verticillioides is an excellent candidate for investigating the potential impact of HGT on the expansion of metabolic activities given that the fungus is soilborne and has a versatile lifestyle as both a symptomless fungus infecting corn and as a pathogen that can cause various diseases on the corn plant. We found strong support that 37 F. verticillioides genes were acquired via HGT, with the great majority of them originating from bacteria. These genes are thought to be involved with different biochemical activities. One of the horizontally transferred genes was highly and specifically expressed when the fungus was challenged with nitric oxide (NO), which is a common antimicrobial defensive compound produced by plants. Detailed analysis suggested the gene moderately enhanced NO-triggered protective responses in F. verticillioides and suppressed expression of the genes responsible for production of the mycotoxin known as fusarin C. Overall, our analysis of HGT events in F. verticillioides supports the hypothesis that HGT offers a mechanism by which fungi can expand their metabolic capabilities, which in turn may enhance their ability to adapt and survive in changing environments. Understanding such adaptation and survival mechanisms may ultimately enhance our ability to control these plant pathogens and the mycotoxins that they produce.

Technical Abstract: Horizontal gene transfer (HGT) is believed to shape genomes by facilitating the rapid acquisition of adaptive traits. We hypothesized that the economically important fungus Fusarium verticillioides is an excellent candidate for investigating the potential impact of HGT on the expansion of metabolic activities given its soilborne nature and versatile lifestyle as both a symptomless endophyte as well as a maize pathogen. To test this hypothesis, we used a phylogenomic pipeline followed by two tiers of manual curation to perform a genome-wide identification of extra-kingdom derived HGT events. We found strong support for 37 gene acquisitions via HGT, 36 of which were putatively from bacteria and one from oomycetes. Functional enrichment assessment of these 37 candidates suggested HGT potentially influenced several biochemical activities, including lysine, glycine and nitrogen metabolism. The expression of 26 candidate HGT genes was detected among RNA-Seq datasets from normal and various stress-related growth conditions, thus indicating potential functionality. FVEG_10494, one of the HGT candidates with homologs in only a few Fusarium species, was highly and specifically up-regulated under nitric oxide (NO) challenge. Functional analysis of FVEG_10494 suggests the gene moderately enhanced NO-triggered protective responses and suppressed expression of the F. verticillioides secondary metabolism gene cluster responsible for production of fusarin C. Overall, our global analysis of HGT events in F. verticillioides identified a core set of transferred genes, raising the hypothesis that HGT offers a mechanism by which fungi can expand their metabolic capabilities, which in turn may enhance their adaptive strategies.