The Yeast Genomics* lab @ NOVA

(*evolutionary, functional, comparative and more)

At the yeast genomics lab @NOVA we have a long-standing interest in various research topics related to sugar transport in yeasts (Saccharomycotina), often with potential industrial applications in view.

Metabolic engineering of industrial yeast strains frequently involves optimization of the sugar transport step, a consequence of the fact that this step has been found to be rate limiting in processes of such importance as bioethanol production and wine and beer fermentations.

In this context, we have isolated and characterized transporters with unique biochemical properties, which may be useful for metabolic engineering.

Fsy1 (Gonçalves et al., 2000), for example, was the first specific fructose transporter to be identified in fungi. Gxs1 and Gxf1 from the yeast Candida intermedia (Leandro et al., 2006) were the first eukaryotic glucose/xylose transporters successfully expressed in Saccharomyces cerevisiae and have been since used for the improvement of bioethanol production from lignocellulosic materials.

Spurred by the high impact of sugar transport on yeast metabolism, we more recently became very interested in the dynamics of the evolution of sugar transporter genes in the Saccharomycotina. While exploring this topic, we found multiple events of horizontal gene transfer, intriguing gene family expansions, as well as strikingly frequent gene losses involving different types of sugar transporters. This line of research employs a combination of comparative genomics anchored on de novo sequencing of relevant genomes, with functional characterization of novel transporters (see highlighted study below).

Presently, our main focus of interest is the molecular basis of fructophily in Saccharomycotina yeasts. Fructophily is intimately linked with a very particular sugar transporter named Ffz1 (Pina et al., 2004), which has apparently evolved from a family of drug-proton antiporters. So far, yeast species found to be fructophilic always harbor a gene encoding an Ffz1 homolog. We are currently investigating multiple aspects of the physiology of fructophilic yeast species as well as the evolutionary history of the Ffz gene family. Our results so far uncovered several HGT events that are probably at the basis of the origin of fructophily in yeasts. We propose that fructophily is likely to have originated as an adaptation to the floricolous niche (to be submitted for publication very soon).

Function and Evolution of Sugar Transporters

Paula Gonçalves

We report in PLoS Genetics our findings concerning the evolutionary trajectory of a single fungal gene encoding a fructose transporter (FSY1) with unique substrate selectivity. A survey that included 241 fungal genomes led to the identification of 109 FSY1 homologues, exclusively found in two of the three major lineages of the phylum Ascomycota. Strikingly, at least 10 independent events of inter-species horizontal gene transfer (HGT) involving FSY1 were detected, which were supported by strong phylogenetic evidence and synteny analyses. We argue that the turbulent evolutionary history of this gene may be related to the unique biochemical proprieties of the encoded transporter, which can be both very useful and detrimental for the host, depending on genetic background and environment. Our results suggest that exchange of genes between fungal species may happen more frequently and may contribute much more substantially to shape fungal genomes than heretofore assumed.

   (read the full story here)

Turbulent evolutionary history of a fungal fructose transporter gene

(A) Species phylogeny and FSY1 ancestral state reconstruction. (B) Symporter activity of Fsy1 homologs of various origins expressed as sole hexose transporter in a S. cerevisiae hxt-null. (C) Growth of the hxt-null strain expressing Fsy1 homologs on medium containing fructose, glucose or maltose as sole carbon and energy source. The overall biochemical properties of Fsy1 homologs of various origins attest conservation of Fsy1 function across a broad phylogenetic range.

Stepwise Functional Evolution in a Fungal Sugar Transporter Family

We report in Molecular Biology and Evolution our findings concerning the relatively recent emergence of a unique family of fungal sugar facilitators, related to drug antiporters. The former transporters, named Ffz, were previously shown to be required for fructophilic metabolism in yeasts. We first exploited the wealth of fungal genomic data available to define a comprehensive but well-delimited family of Ffz-like transporters, showing that they are only present in Dikarya. Subsequently, a combination of phylogenetic analyses and in vivo functional characterization was used to retrace important changes in function, while highlighting the evolutionary events that are most likely to have determined extant distribution of the gene, such as horizontal gene transfers (HGTs). One such HGT event is proposed to have set the stage for the onset of fructophilic metabolism in yeasts, a trait that according to our results may be the metabolic hallmark of close to 100 yeast species that thrive in sugar rich environments.

   (read the full story here)

Evidence for intra-kingdom HGT in the evolution of the FFZ family

Functional analysis of Ffz homologs expressed as sole hexose transporters in S. cerevisiae hxt-null.

Glucose and fructose consumption profiles of Wickerhamiella species

Prevalence of Ffz in Dikarya

(presence in black, absence in white)