Contrasting Strategies for Sucrose Utilization in a Floral Yeast Clade

This work was financed by national funds from FCT—Fundação para a Ciência e a Tecnologia, I.P. (FCT/MCTES; https://www.fct.pt/), in the scope of project UIDP/04378/ 2020 and UIDB/04378/2020 of the Research Unit on Applied Molecular Biosciences— UCIBIO and project LA/P/0140/2020 of the Associate Laboratory Institute for Health and Bioeconomy—i4HB and also was supported by grants FructYEAST—LISBOA-01-0145-FEDER-029529/PTDC/BIA-MIC/29529/2017 (to P.G.) and PTDC/BIA-EVL/1100/2020 (to P.G.), both from FCT/MCTES.Yeast species in the Wickerhamiella and Starmerella genera (W/S clade) thrive in the sugar-rich floral niche. We have previously shown that species belonging to this clade harbor an unparalleled number of genes of bacterial origin, among which is the SUC2 gene, encoding a sucrose-hydrolyzing enzyme. In this study, we used complementary in silico and experimental approaches to examine sucrose utilization in a broader cohort of species representing extant diversity in the W/S clade. Distinct strategies and modes of sucrose assimilation were unveiled, involving either extracellular sucrose hydrolysis through secreted bacterial Suc2 or intracellular assimilation using broad-substrate-range α-glucoside/H+ symporters and α-glucosidases. The intracellular pathway is encoded in two types of gene clusters reminiscent of the MAL clusters in Saccharomyces cerevisiae, where they are involved in maltose utilization. The genes composing each of the two types of MAL clusters found in the W/S clade have disparate evolutionary histories, suggesting that they formed de novo. Both transporters and glucosidases were shown to be functional and additionally involved in the metabolization of other disaccharides, such as maltose and melezitose. In one Wickerhamiella species lacking the α-glucoside transporter, maltose assimilation is accomplished extracellularly, an attribute which has been rarely observed in fungi. Sucrose assimilation in Wickerhamiella generally escaped both glucose repression and the need for an activator and is thus essentially constitutive, which is consistent with the abundance of both glucose and sucrose in the floral niche. The notable plasticity associated with disaccharide utilization in the W/S clade is discussed in the context of ecological implications and energy metabolism. IMPORTANCE Microbes usually have flexible metabolic capabilities and are able to use different compounds to meet their needs. The yeasts belonging to the Wickerhamiella and Starmerella genera (forming the so-called W/S clade) are usually found in flowers or insects that visit flowers and are known for having acquired many genes from bacteria by a process called horizontal gene transfer. One such gene, dubbed SUC2, is used to assimilate sucrose, which is one of the most abundant sugars in floral nectar. Here, we show that different lineages within the W/S clade used different solutions for sucrose utilization that dispensed SUC2 and differed in their energy requirements, in their capacity to scavenge small amounts of sucrose from the environment, and in the potential for sharing this resource with other microbial species. We posit that this plasticity is possibly dictated by adaptation to the specific requirements of each species.publishersversionpublishe

Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae

This work was supported by Fundacao para a Ciencia e a Tecnologia, Portugal, grants PTDC/BIA-EVF/118618/2010 (J.P.S., P.A., P.G.), PTDC/AGR-ALI/118590/2010 (J.P.S., P.A., P.G., R.B.), UID/Multi/04378/2013 (J.P.S., P.G.), and SFRH/BD/77390/2011 (P.A.), by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico-CNPq (CAR, process numbers 560715/2010-2 and 457499/2014-1, PBM process number 457443/2012-0) and Fundacao de Amparo a Pesquisa de Minas Gerais FAPEMIG and VALE S.A (CAR, process number RCP-00094-10). Work of C.R.L. on this project was supported by a NSERC Discovery grant. C.R.L. holds the Canada Research Chair in Evolutionary Cell and Systems Biology. The authors thank Dr. Siu Mui Tsai, Universidade de Sao Paulo, Brazil, for making available strain UFMG-CM-Y640.The natural biology of Saccharomyces cerevisiae, the best known unicellular model eukaryote, remains poorly documented and understood although recent progress has started to change this situation. Studies carried out recently in the Northern Hemisphere revealed the existence of wild populations associated with oak trees in North America, Asia, and in the Mediterranean region. However, in spite of these advances, the global distribution of natural populations of S. cerevisiae, especially in regions were oaks and other members of the Fagaceae are absent, is not well understood. Here we investigate the occurrence of S. cerevisiae in Brazil, atropical region where oaks and other Fagaceae are absent. We report a candidate natural habitat of S. cerevisiae in South America and, using whole-genome data, we uncover new lineages that appear to have as closest relatives the wild populations found in North America and Japan. A population structure analysis revealed the penetration of the wine genotype into the wild Brazilian population, a first observation of the impact of domesticated microbe lineages on the genetic structure of wild populations. Unexpectedly, the Brazilian population shows conspicuous evidence of hybridization with an American population of Saccharomyces paradoxus. Introgressions from S. paradoxus were significantly enriched in genes encoding secondary active transmembrane transporters. We hypothesize that hybridization in tropical wild lineages may have facilitated the habitat transition accompanying the colonization of the tropical ecosystem.publishersversionpublishe