Abstract
In the past decade, the sequencing of large cohorts of Saccharomyces cerevisiae strains has revealed a landscape of genomic regions acquired by Horizontal Gene Transfer (HGT). The genes acquired by HGT play important roles in yeast adaptation to the fermentation process, improving nitrogen and carbon source utilization. However, the functional characterization of these genes at the molecular level has been poorly attended. In this work, we carried out a systematic analysis of the promoter activity and protein level of 30 genes contained in three horizontally acquired regions commonly known as regions A, B, and C. In three strains (one for each region), we used the luciferase reporter gene and the mCherry fluorescent protein to quantify the transcriptional and translational activity of these genes, respectively. We assayed the strains generated in four different culture conditions; all showed low levels of transcriptional and translational activity across these environments. However, we observed an increase in protein levels under low nitrogen culture conditions, suggesting a possible role of the horizontally acquired genes in the adaptation to nitrogen-limited environments. Furthermore, since the strains carrying the luciferase reporter gene are null mutants for the horizontally acquired genes, we assayed growth parameters (latency time, growth rate, and efficiency) and the fermentation kinetics in this set of deletion strains. The results showed that single deletion of 20 horizontally acquired genes modified the growth parameters, whereas the deletion of five of them altered the maximal CO2 production rate (Vmax). Interestingly, we observed a correlation between growth parameters and Vmax for an ORF within region A, encoding an ortholog to a thiamine (vitamin B1) transporter whose deletion decreased the growth rate, growth efficiency, and CO2 production. Altogether, our results provided molecular and phenotypic evidence highlighting the importance of horizontally acquired genes in yeast adaptation to fermentative environments.
Highlights
The widespread use of the budding yeast Saccharomyces cerevisiae as a eukaryotic model organism led to the sequencing of the genome of this microorganism more than 20 years ago (Goffeau et al, 1996)
These genetic hallmarks are frequently absent in the yeast reference genome and, in general, they have been acquired by introgression from a closely related species or by Horizontal Gene Transfer (HGT) from a more distant species (Morales and Dujon, 2012)
The contribution of the HGT process in the configuration of eukaryotic genomes is receiving renewed attention, especially in S. cerevisiae, where large-scale sequencing projects have revealed that HGT is a very extensive phenomenon (Legras et al, 2018; Peter et al, 2018)
Summary
The widespread use of the budding yeast Saccharomyces cerevisiae as a eukaryotic model organism led to the sequencing of the genome of this microorganism more than 20 years ago (Goffeau et al, 1996). The variety of sequenced strains includes isolates from domesticated settings, such as vineyards, breweries, cheese, dairy, and clinical environments as well as wild strains isolated from nondomesticated environments, such as forests, flowers, and tree bark (Liti et al, 2009; Novo et al, 2009; Borneman et al, 2011; Wang et al, 2012; Bergström et al, 2014; Strope et al, 2015; Legras et al, 2018; Peter et al, 2018) In this sense, the “1002 yeast genomes project” is the most comprehensive collection of the genetic variation of yeast, encompassing the genome information of 1011 isolates from diverse geographical origins and ecological niches and describing 26 clades within the yeast population structure (Peter et al, 2018). Detection of HGT is performed by phylogenetic methods to identify genes with a different evolutionary trajectory with respect to the host genes (Roelofs and Van Haastert, 2001; Keeling and Palmer, 2008; Ravenhall et al, 2015)
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