Emergence of Species-Specific Transporters during Evolution of the Hemiascomycete Phylum

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ABSTRACT

We have traced the evolution patterns of 2480 transmembrane transporters from five complete genome sequences spanning the entire Hemiascomycete phylum: Saccharomyces cerevisiae, Candida glabrata, Kluyveromyces lactis, Debaryomyces hansenii, and Yarrowia lipolytica. The use of nonambiguous functional and phylogenetic criteria derived from the TCDB classification system has allowed the identification within the Hemiascomycete phylum of 97 small phylogenetic transporter subfamilies comprising a total of 355 transporters submitted to four distinct evolution patterns named "ubiquitous," "species specific," "phylum gains and losses," or "homoplasic." This analysis identifies the transporters that contribute to the emergence of species during the evolution of the Hemiascomycete phylum and may aid in establishing novel phylogenetic criteria for species classification.

THE Hemiascomycete yeasts are believed to have diverged from a common ancestral fungus at least 400 million years ago. This phylum comprises >1200 known species (KURTZMAN and FELL 1998; BOEKHOUT 2005). The first Hemiascomycete genome sequence, that of Saccharomyces cerevisiae, has unraveled the existence of >30% of duplicated genes. This observation led to the hypothesis of a recent whole-genome duplication of the Saccharomyces genome (PHILIPPSEN et al. 1997; WOLFE and SHIELDS 1997). A massive exploration of partially sequenced genomes from 13 Hemiascomycete species (SouciET et al. 2000) as well as the sequence comparison of a selected set of 40 duplicated gene sequences from six different species further investigated the origin of duplicated genes within the Hemiascomycete phylum (LANGKJAER et al. 2003). Analysis of several nearly complete genome sequences from Hemiascomycete species closely related to S. cerevisiae has dated the whole-genome duplication after the emergence of Kluyveromyces waltii (KELLIS et al. 2004), Ashbya gossypii (DIETRICH et al. 2004), and K. lactis (DujON et al. 2004) but before that of all sensus stricto and sensus lato Saccharomyces species (CLIFTEN et al. 2003; KELLIS et al. 2003) and Candida glabrata (DujON et al. 2004). Thèse data established the high frequency of gene loss among the duplicated genes. The existence in fungi of numerous gene duplication events followed by differential evolutionary drift of one of the two gene copies is believed to be a major force for adaptation to novel ecological niches and further speciation (OHNO 1970; KELLIS et al. 2003; LANGKJAER et al. 2003; DUJON et al. 2004).

The complete genome sequence of four species widely spread over the Hemiascomycete phylum became recently available: C. glabrata, the second most prominent causative agent of human fungal infection; K. lactis, a milk-loving yeast, believed to have diverged from the Saccharomyces clade at least 150 millions years ago; Debaromyces hansenii, a halotolerant species contaminating many dairy products; and Yarrowia lipolytica, a distantly related yeast that shares a number of properties with filamentous fungi (DujON et al. 2004). In the context of this Genolevures project, a uniform nomenclature was designed to facilitate comparisons between species (DURRENS and SHERMAN 2005). These data established that in addition to a recent whole-genome duplication, variable levels of segmentai duplication, tandem repeats, and other duplication events of still unknown mechanisms have occurred during evolution of the Hemiascomycete phylum. The analyses of more ancient genomes such as those from the major human Hemiascomycete pathogen C. albicans (JONES et al. 2004) and from the Euascomycete filamentous fungus Neurospora crassa (GALAGAN et al. 2003) are fully consistent with this view.

Most of the gene products and gene families analyzed so far concerned nonmembrane proteins or RNAs. We wish to focus our analysis here on the evolutionary fate of transmembrane transporter proteins that correspond to ~10% of the coding genes in the Hemiascomycete phylum. …