Comparative genomics revealed in the last decade a scenario of rampant horizontal gene transfer (HGT) among prokaryotes, but for fungi a clearly dominant pattern of vertical inheritance still stands, punctuated however by an increasing number of exceptions. In the present work, we studied the phylogenetic distribution and pattern of inheritance of a fungal gene encoding a fructose transporter (FSY1) with unique substrate selectivity. 109 FSY1 homologues were identified in two sub-phyla of the Ascomycota, in a survey that included 241 available fungal genomes. At least 10 independent inter-species instances of horizontal gene transfer (HGT) involving FSY1 were identified, supported by strong phylogenetic evidence and synteny analyses. The acquisition of FSY1 through HGT was sometimes suggestive of xenolog gene displacement, but several cases of pseudoparalogy were also uncovered. Moreover, evidence was found for successive HGT events, possibly including those responsible for transmission of the gene among yeast lineages. These occurrences do not seem to be driven by functional diversification of the Fsy1 proteins because Fsy1 homologues from widely distant lineages, including at least one acquired by HGT, appear to have similar biochemical properties. In summary, retracing the evolutionary path of the FSY1 gene brought to light an unparalleled number of independent HGT events involving a single fungal gene. We propose that the turbulent evolutionary history of the gene may be linked to the unique biochemical properties of the encoded transporter, whose predictable effect on fitness may be highly variable. In general, our results support the most recent views suggesting that inter-species HGT may have contributed much more substantially to shape fungal genomes than heretofore assumed.
Genes are commonly vertically inherited, meaning that they share the evolutionary history of the organisms in which they are found. However, they can also be transmitted between species with overlapping niches, a phenomenon known as horizontal gene transfer (HGT) that can occur between closely related species but also between organisms belonging to different domains of life. While HGT is very common in prokaryotes, it has been less frequently reported in eukaryotes, including eukaryotic microbes. In fungi, several instances of genes acquired by HGT from bacteria have been reported, but gene exchange between fungal species is thought to be rare. Here, we describe our findings concerning a single fungal gene that seems to have been transferred between fungi very often. We believe this may be related to the fact that the gene can be both very useful and detrimental for the host, depending on genetic background and environment. Our results suggest that exchange of genes between fungi may happen much more frequently than assumed so far.