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Contrasting Strategies for Sucrose Utilization in a Floral Yeast Clade
Publication . Gonçalves, Carla; Marques, Margarida; Gonçalves, Paula Maria Theriaga Mendes Bernardo; UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; American Society for Microbiology
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.
Tracking alternative versions of the galactose gene network in the genus Saccharomyces and their expansion after domestication
Publication . Pontes, Ana; Paraíso, Francisca; Liu, Yu Ching; Limtong, Savitree; Jindamorakot, Sasitorn; Jespersen, Lene; Gonçalves, Carla; Rosa, Carlos A.; Tsai , Isheng Jason; Rokas, Antonis; Hittinger, Chris Todd; Gonçalves, Paula; Sampaio, José Paulo; UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; Elsevier
When Saccharomyces cerevisiae grows on mixtures of glucose and galactose, galactose utilization is repressed by glucose, and induction of the GAL gene network only occurs when glucose is exhausted. Contrary to reference GAL alleles, alternative alleles support faster growth on galactose, thus enabling distinct galactose utilization strategies maintained by balancing selection. Here, we report on new wild populations of Saccharomyces cerevisiae harboring alternative GAL versions and, for the first time, of Saccharomyces paradoxus alternative alleles. We also show that the non-functional GAL version found earlier in Saccharomyces kudriavzevii is phylogenetically related to the alternative versions, which constitutes a case of trans-specific maintenance of highly divergent alleles. Strains harboring the different GAL network variants show different levels of alleviation of glucose repression and growth proficiency on galactose. We propose that domestication involved specialization toward thriving in milk from a generalist ancestor partially adapted to galactose consumption in the plant niche.
Extensive remodeling of sugar metabolism through gene loss and horizontal gene transfer in a eukaryotic lineage
Publication . Pontes, Ana; Paraíso, Francisca; Silva, Margarida; Lagoas, Catarina; Aires, Andreia; Brito, Patrícia H.; Rosa, Carlos A.; Lachance, Marc André; Sampaio, José Paulo; Gonçalves, Carla; Gonçalves, Paula; UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; Faculdade de Ciências e Tecnologia (FCT); Springer Verlag
Background: In yeasts belonging to the subphylum Saccharomycotina, genes encoding components of the main metabolic pathways, like alcoholic fermentation, are usually conserved. However, in fructophilic species belonging to the floral Wickerhamiella and Starmerella genera (W/S clade), alcoholic fermentation was uniquely shaped by events of gene loss and horizontal gene transfer (HGT). Results: Because HGT and gene losses were first identified when only eight W/S-clade genomes were available, we collected publicly available genome data and sequenced the genomes of 36 additional species. A total of 63 genomes, representing most of the species described in the clade, were included in the analyses. Firstly, we inferred the phylogenomic tree of the clade and inspected the genomes for the presence of HGT-derived genes involved in fructophily and alcoholic fermentation. We predicted nine independent HGT events and several instances of secondary loss pertaining to both pathways. To investigate the possible links between gene loss and acquisition events and evolution of sugar metabolism, we conducted phenotypic characterization of 42 W/S-clade species including estimates of sugar consumption rates and fermentation byproduct formation. In some instances, the reconciliation of genotypes and phenotypes yielded unexpected results, such as the discovery of fructophily in the absence of the cornerstone gene (FFZ1) and robust alcoholic fermentation in the absence of the respective canonical pathway. Conclusions: These observations suggest that reinstatement of alcoholic fermentation in the W/S clade triggered a surge of innovation that goes beyond the utilization of xenologous enzymes, with fructose metabolism playing a key role.
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Fundação para a Ciência e a Tecnologia
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3599-PPCDT
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PTDC/BIA-EVL/1100/2020