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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.
Diverse signatures of convergent evolution in cactus-associated yeasts
Publication . Gonçalves, Carla; Harrison, Marie Claire; Steenwyk, Jacob L.; Opulente, Dana A.; LaBella, Abigail L.; Wolters, John F.; Zhou, Xiaofan; Shen, Xing Xing; Groenewald, Marizeth; Hittinger, Chris Todd; Rokas, Antonis; Faculdade de Ciências e Tecnologia (FCT); UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; Public Library of Science
AU Many: Pleaseconfirmthatallheadinglevelsarerepresentedcorrectly distantly related organisms have convergently evolved: traits and lifestyles that enable them to live in similar ecological environments. However, the extent of phenotypic convergence evolving through the same or distinct genetic trajectories remains an open question. Here, we leverage a comprehensive dataset of genomic and phenotypic data from 1,049 yeast species in the subphylum Saccharomycotina (Kingdom Fungi, Phylum Ascomycota) to explore signatures of convergent evolution in cactophilic yeasts, ecological specialists associated with cacti. We inferred that the ecological association of yeasts with cacti arose independently approximatelyAU 17 times.: PleasenotethatasperPLOSstyle Using a machine learning–based ; donotusethesymbol approach, we inprosetomeanabo further found that cactophily can be predicted with 76% accuracy from both functional genomic and phenotypic data. The most informative feature for predicting cactophily was thermotolerance, which we found to be likely associated with altered evolutionary rates of genes impacting the cell envelope in several cactophilic lineages. We also identified horizontal gene transfer and duplication events of plant cell wall–degrading enzymes in distantly related cactophilic clades, suggesting that putatively adaptive traits evolved independently through disparate molecular mechanisms. Notably, we found that multiple cactophilic species and their close relatives have been reported as emerging human opportunistic pathogens, suggesting that the cactophilic lifestyle—and perhaps more generally lifestyles favoring thermotolerance—might preadapt yeasts to cause human disease. This work underscores the potential of a multifaceted approach involving high-throughput genomic and phenotypic data to shed light onto ecological adaptation and highlights how convergent evolution to wild environments could facilitate the transition to human pathogenicity.
Convergent reductive evolution in bee-associated lactic acid bacteria
Publication . Pontes, Ana; Harrison, Marie Claire; Rokas, Antonis; Gonçalves, Carla; Faculdade de Ciências e Tecnologia (FCT); UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; American Society for Microbiology
Distantly related organisms may evolve similar traits when exposed to similar environments or engaging in certain lifestyles. Several members of the Lactobacillaceae [lactic acid bacteria (LAB)] family are frequently isolated from the floral niche, mostly from bees and flowers. In some floral LAB species (henceforth referred to as bee-associated LAB), distinctive genomic (e.g., genome reduction) and phenotypic (e.g., preference for fructose over glucose or fructophily) features were recently documented. These features are found across distantly related species, raising the hypothesis that specific genomic and phenotypic traits evolved convergently during adaptation to the floral environment. To test this hypothesis, we examined representative genomes of 369 species of bee-associated and non-bee-associated LAB. Phylogenomic analysis unveiled seven independent ecological shifts toward the bee environment in LAB. In these species, we observed significant reductions of genome size, gene repertoire, and GC content. Using machine leaning, we could distinguish bee-associated from non-bee-associated species with 94% accuracy, based on the absence of genes involved in metabolism, osmotic stress, or DNA repair. Moreover, we found that the most important genes for the machine learning classifier were seemingly lost, independently, in multiple bee-associated lineages. One of these genes, acetaldehyde–alcohol dehydrogenase (adhE), encodes a bifunctional aldehyde–alcohol dehydrogenase which has been associated with the evolution of fructophily, a rare phenotypic trait that is pervasive across bee-associated LAB species. These results suggest that the independent evolution of distinctive phenotypes in bee-associated LAB has been largely driven by independent losses of the same sets of genes.
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Fundação para a Ciência e a Tecnologia
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3599-PPCDT
Número da atribuição
PTDC/BIA-EVL/0604/2021