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

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 manual curation to perform a genome-wide identification of inter-kingdom derived HGT events. We found strong support for 36 genes in F. verticillioides putatively acquired from bacteria. Functional enrichment assessment of these 36 candidates suggested HGT potentially influenced several biochemical activities, including lysine, glycine and nitrogen metabolism. The expression of 25 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 well-supported set of transferred genes, providing further evidence that HGT offers a mechanism by which fungi can expand their metabolic capabilities, which in turn may enhance their adaptive strategies.