Abstract
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.
Highlights
Gene gain and loss are deemed to be important mechanisms underlying adaptation to different lifestyles across all domains of life
Whereas it is commonly accepted that vertical descent with modification as well as gene duplication followed by divergence of the resulting paralogous genes are paramount for the expansion of gene diversity in prokaryotes, horizontal gene transfer (HGT) between species follows closely in importance, since it seems to have been a very frequent source of genetic novelty throughout the evolution of both Archaea and Bacteria [2,3]
Genes are commonly vertically inherited, meaning that they share the evolutionary history of the organisms in which they are found. They can be transmitted between species with overlapping niches, a phenomenon known as horizontal gene transfer (HGT) that can occur between closely related species and between organisms belonging to different domains of life
Summary
Gene gain and loss are deemed to be important mechanisms underlying adaptation to different lifestyles across all domains of life For many prokaryotes this reflects in the relative sizes of the ‘‘core genome’’, shared by all individuals of a species, and the so called accessory genome that equips the cells for survival in specific environments and can represent as much as 60% of the total genome [1]. This plasticity is generally thought to be related to the relative ease with which prokaryotes are able to discard genes that are not required, as well as to the diversity and effectiveness of mechanisms mediating gene acquisition [2]. The ‘‘resident’’ gene seemed to have been replaced by a homolog acquired from a different species, an event dubbed ‘‘xenolog gene displacement’’ [2]
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