RESUMEN
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.
Asunto(s)
Transferencia de Gen Horizontal , Filogenia , Metabolismo de los Hidratos de Carbono/genética , Azúcares/metabolismo , Evolución Molecular , Genoma FúngicoRESUMEN
Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Two general paradigms have been proposed to explain this variation: (i) trade-offs between performance efficiency and breadth and (ii) the joint influence of extrinsic (environmental) and intrinsic (genomic) factors. We assembled genomic, metabolic, and ecological data from nearly all known species of the ancient fungal subphylum Saccharomycotina (1154 yeast strains from 1051 species), grown in 24 different environmental conditions, to examine niche breadth evolution. We found that large differences in the breadth of carbon utilization traits between yeasts stem from intrinsic differences in genes encoding specific metabolic pathways, but we found limited evidence for trade-offs. These comprehensive data argue that intrinsic factors shape niche breadth variation in microbes.
Asunto(s)
Ascomicetos , Carbono , Interacción Gen-Ambiente , Nitrógeno , Ascomicetos/clasificación , Ascomicetos/genética , Ascomicetos/metabolismo , Carbono/metabolismo , Genoma Fúngico , Redes y Vías Metabólicas/genética , Nitrógeno/metabolismo , FilogeniaRESUMEN
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.
RESUMEN
Two novel ascomycetous yeast species of the genus Wickerhamiella are proposed based on isolates obtained in Thailand from food waste and the fruiting body of a polypore fungus, and on a combination of conventional DNA-barcode sequence analyses and whole-genome phylogenies. We focus on a particular subclade of the genus Wickerhamiella that contains species found in anthropic environments and describe Wickerhamiella limtongiae sp. nov. (DMKU-FW31-5T=PYCC 9022T=TBRC 15055T), found on food waste samples. In an adjacent clade, we describe Wickerhamiella koratensis sp. nov. (DMKU-KO16T=PYCC 8908T=TBRC 14869T), which represents the closest relative of Wickerhamiella slavikovae and was isolated from the fruiting body of Bjerkandera sp. In the subclade of W. limtongiae sp. nov., we propose that Wickerhamiella infanticola should be regarded as a synonym of Wickerhamiella sorbophila and that Wickerhamiella tropicalis should be regarded as a synonym of Wickerhamiella verensis.
Asunto(s)
Eliminación de Residuos , Saccharomycetales , Filogenia , Alimentos , Análisis de Secuencia de ADN , ADN de Hongos/genética , Técnicas de Tipificación Micológica , Composición de Base , ARN Ribosómico 16S/genética , ADN Bacteriano/genética , Técnicas de Tipificación Bacteriana , Ácidos Grasos/química , TailandiaRESUMEN
Four yeast isolates collected from flowers from different ecosystems in Brazil, one from fruit of Nothofagus alpina in Argentina, three from flowers of Neltuma chilensis in Chile and one obtained from the proventriculus of a female bumblebee in Canada were demonstred, by analysis of the sequences of the internal transcribed spacer (ITS) region and D1/D2 domains of the large subunit rRNA gene, to represent two novel species of the genus Starmerella. These species are described here as Starmerella gilliamiae f.a, sp. nov. (CBS 16166T; Mycobank MB 851206) and Starmerella monicapupoae f.a., sp. nov. (PYCC 8997T; Mycobank MB 851207). The results of a phylogenomic analysis using 1037 single-copy orthogroups indicated that S. gilliamiae is a member of a subclade that contains Starmerella opuntiae, Starmerella aceti and Starmerella apicola. The results also indicated that S. monicapupoae is phylogenetically related to Starmerella riodocensis. The two isolates of S. monicapupoae were obtained from flowers in Brazil and were probably vectored by insects that visit these substrates. Starmerella gilliamiae has a wide geographical distribution having been isolated in flowers from Brazil and Chile, fruit from Argentina and a bumblebee from Canada.
Asunto(s)
Ecosistema , Saccharomycetales , Animales , Filogenia , Análisis de Secuencia de ADN , ARN Ribosómico 16S/genética , ADN Bacteriano/genética , Técnicas de Tipificación Bacteriana , Composición de Base , Ácidos Grasos/química , Saccharomycetales/genética , InsectosRESUMEN
The inebriation of wild African elephants from eating the ripened and rotting fruit of the marula tree is a persistent myth in Southern Africa. However, the yeasts responsible for alcoholic fermentation to intoxicate the elephants remain poorly documented. In this study, we considered Botswana, a country with the world's largest population of wild elephants, and where the marula tree is indigenous, abundant and protected, to assess the occurrence and biodiversity of yeasts with a potential to ferment and subsequently inebriate the wild elephants. We collected marula fruits from over a stretch of 800 km in Botswana and isolated 106 yeast strains representing 24 yeast species. Over 93% of these isolates, typically known to ferment simple sugars and produce ethanol comprising of high ethanol producers belonging to Saccharomyces, Brettanomyces, and Pichia, and intermediate ethanol producers Wickerhamomyces, Zygotorulaspora, Candida, Hanseniaspora, and Kluyveromyces. Fermentation of marula juice revealed convincing fermentative and aromatic bouquet credentials to suggest the potential to influence foraging behaviour and inebriate elephants in nature. There is insufficient evidence to refute the aforementioned myth. This work serves as the first work towards understanding the biodiversity marula associated yeasts to debunk the myth or approve the facts.
RESUMEN
Certain lineages of the wine, beer and bread yeast Saccharomyces cerevisiae have diastatic activity. They contain the chimeric gene STA1 that codes for an extracellular glucoamylase which enables the strains to degrade starch and dextrins. Beer contaminations by diastatic yeasts can be dangerous because they can cause super-attenuation due to the consumption of otherwise non-fermentable oligosaccharides, gushing and off-flavours. Given that diastatic yeasts can be used for beer fermentation it is important to understand the relationship between production and contaminant strains, their natural reservoirs and entry routes into the brewery. Here, we analyze real cases of contamination in a Portuguese craft brewery over a period of 18 months. By analyzing with whole genome sequencing several contaminants, we show that recurrent contaminations by diastatic yeasts are caused by environmental strains. Moreover, some beer contaminants were closely related to diastatic environmental strains isolated in Botswana. We observed the widespread presence of domestication signatures in diastatic strains. Moreover, the combined phylogeny of STA1 and its ancestor, SGA1, suggested a single STA1 origin, as ancient as the entire lineage of diastatic yeasts. Together, our results suggest that diastatic yeasts isolated in natural settings could be escaping from domestication settings and becoming feral.
RESUMEN
Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Paradigms proposed to explain this variation either invoke trade-offs between performance efficiency and breadth or underlying intrinsic or extrinsic factors. We assembled genomic (1,154 yeast strains from 1,049 species), metabolic (quantitative measures of growth of 843 species in 24 conditions), and ecological (environmental ontology of 1,088 species) data from nearly all known species of the ancient fungal subphylum Saccharomycotina to examine niche breadth evolution. We found large interspecific differences in carbon breadth stem from intrinsic differences in genes encoding specific metabolic pathways but no evidence of trade-offs and a limited role of extrinsic ecological factors. These comprehensive data argue that intrinsic factors driving microbial niche breadth variation.
RESUMEN
During a survey of floricolous yeasts in Portugal, a basidiomycetous yeast representing a novel species in the genus Hannaella was isolated in Portugal from the flower of Lantana camara, an ornamental exotic species native to Central and South America. A combination of phylogenetic analyses of DNA barcode sequences used in yeast molecular systematics, namely the D1/D2 domain and the complete internal transcribed spacer (ITS) region supported the recognition of a new species of Hannaella, that we designate Hannaella floricola sp. nov. (ex-type strain PYCC 9191T=CBS 18097T). Although the assignment of the new species to the genus Hannaella was evident, the detection of its closest relatives appeared more problematic. Nevertheless, our analyses suggested that H. floricola sp. nov. belongs a clade that also includes H. coprosmae, H. oryzae and H. surugaensis, together four candidate novel species. In addition we provide the molecular identification of several unidentified strains whose D1/D2 and ITS sequences are available from GenBank.
Asunto(s)
Ascomicetos , Basidiomycota , Lantana , ADN de Hongos/genética , Lantana/genética , Filogenia , Portugal , ADN Espaciador Ribosómico/genética , ARN Ribosómico 16S/genética , Análisis de Secuencia de ADN , Técnicas de Tipificación Micológica , ADN Bacteriano/genética , Técnicas de Tipificación Bacteriana , Composición de Base , Ácidos Grasos/química , Ascomicetos/genética , FloresRESUMEN
Species is the fundamental unit to quantify biodiversity. In recent years, the model yeast Saccharomyces cerevisiae has seen an increased number of studies related to its geographical distribution, population structure, and phenotypic diversity. However, seven additional species from the same genus have been less thoroughly studied, which has limited our understanding of the macroevolutionary events leading to the diversification of this genus over the last 20 million years. Here, we show the geographies, hosts, substrates, and phylogenetic relationships for approximately 1,800 Saccharomyces strains, covering the complete genus with unprecedented breadth and depth. We generated and analyzed complete genome sequences of 163 strains and phenotyped 128 phylogenetically diverse strains. This dataset provides insights about genetic and phenotypic diversity within and between species and populations, quantifies reticulation and incomplete lineage sorting, and demonstrates how gene flow and selection have affected traits, such as galactose metabolism. These findings elevate the genus Saccharomyces as a model to understand biodiversity and evolution in microbial eukaryotes.
Asunto(s)
Saccharomyces cerevisiae , Saccharomyces , Saccharomyces cerevisiae/genética , Filogenia , Saccharomyces/genética , Biodiversidad , FenotipoRESUMEN
Microbe domestication has a major applied relevance but is still poorly understood from an evolutionary perspective. The yeast Torulaspora delbrueckii is gaining importance for biotechnology but little is known about its population structure, variation in gene content or possible domestication routes. Here, we show that T. delbrueckii is composed of five major clades. Among the three European clades, a lineage associated with the wild arboreal niche is sister to the two other lineages that are linked to anthropic environments, one to wine fermentations and the other to diverse sources including dairy products and bread dough (Mix-Anthropic clade). Using 64 genomes we assembled the pangenome and the variable genome of T. delbrueckii. A comparison with Saccharomyces cerevisiae indicated that the weight of the variable genome in the pangenome of T. delbrueckii is considerably smaller. An association of gene content and ecology supported the hypothesis that the Mix-Anthropic clade has the most specialized genome and indicated that some of the exclusive genes were implicated in galactose and maltose utilization. More detailed analyses traced the acquisition of a cluster of GAL genes in strains associated with dairy products and the expansion and functional diversification of MAL genes in strains isolated from bread dough. In contrast to S. cerevisiae, domestication in T. delbrueckii is not primarily driven by alcoholic fermentation but rather by adaptation to dairy and bread-production niches. This study expands our views on the processes of microbe domestication and on the trajectories leading to adaptation to anthropic niches.
Asunto(s)
Torulaspora , Vino , Saccharomyces cerevisiae/genética , Torulaspora/genética , Domesticación , Fermentación , Vino/análisisRESUMEN
During studies of yeasts associated with soil in a Cerrado-Atlantic Rain Forest ecotone site in Brazil, three orange-pigmented yeast strains were isolated from samples collected in Minas Gerais state, Brazil. Molecular analyses combining the 26S rRNA gene (D1/D2 domains) and the internal transcribed spacer (ITS) sequences as well as whole-genome sequence data showed that these strains could not be ascribed to any known species in the basidiomycetous genus Phaffia, and thus they are considered to represent a novel species for which the name Phaffia brasiliana sp. nov. is proposed. The holotype is CBS 16121T and the MycoBank number is MB 839315. The occurrence of P. brasiliana in a tropical region is unique for the genus, since all other species occur in temperate regions. Two factors appear to contribute to the distribution of the novel taxon: first, the region where it was found has relatively moderate temperature ranges and, second, an adaptation to grow or withstand temperatures higher than those of the other species in the genus seems to be in place.
Asunto(s)
Basidiomycota/clasificación , Filogenia , Bosque Lluvioso , Microbiología del Suelo , Basidiomycota/aislamiento & purificación , Brasil , ADN de Hongos/genética , ADN Espaciador Ribosómico/genética , Técnicas de Tipificación Micológica , ARN Ribosómico 16S/genética , Análisis de Secuencia de ADNRESUMEN
The unambiguous application of fungal names is important to communicate scientific findings. Names are critical for (clinical) diagnostics, legal compliance, and regulatory controls, such as biosafety, food security, quarantine regulations, and industrial applications. Consequently, the stability of the taxonomic system and the traceability of nomenclatural changes is crucial for a broad range of users and taxonomists. The unambiguous application of names is assured by the preservation of nomenclatural history and the physical organisms representing a name. Fungi are extremely diverse in terms of ecology, lifestyle, and methods of study. Predominantly unicellular fungi known as yeasts are usually investigated as living cultures. Methods to characterize yeasts include physiological (growth) tests and experiments to induce a sexual morph; both methods require viable cultures. Thus, the preservation and availability of viable reference cultures are important, and cultures representing reference material are cited in species descriptions. Historical surveys revealed drawbacks and inconsistencies between past practices and modern requirements as stated in the International Code of Nomenclature for Algae, Fungi, and Plants (ICNafp). Improper typification of yeasts is a common problem, resulting in a large number invalid yeast species names. With this opinion letter, we address the problem that culturable microorganisms, notably some fungi and algae, require specific provisions under the ICNafp. We use yeasts as a prominent example of fungi known from cultures. But viable type material is important not only for yeasts, but also for other cultivable Fungi that are characterized by particular morphological structures (a specific type of spores), growth properties, and secondary metabolites. We summarize potential proposals which, in our opinion, will improve the stability of fungal names, in particular by protecting those names for which the reference material can be traced back to the original isolate.
RESUMEN
The adaptation to the different biotic and abiotic factors of wine fermentation has led to the accumulation of numerous genomic hallmarks in Saccharomyces cerevisiae wine strains. IRC7, a gene encoding a cysteine-S-ß-lyase enzyme related volatile thiols production in wines, has two alleles: a full-length allele (IRC7F ) and a mutated one (IRC7S ), harbouring a 38 bp-deletion. Interestingly, IRC7S -encoding a less active enzyme - appears widespread amongst wine populations. Studying the global distribution of the IRC7S allele in different yeast lineages, we confirmed its high prevalence in the Wine clade and demonstrated a minority presence in other domesticated clades (Wine-PDM, Beer and Bread) while it is completely missing in wild clades. Here, we show that IRC7S -homozygous (HS) strains exhibited both fitness and competitive advantages compared with IRC7F -homozygous (HF) strains. There are some pieces of evidence of the direct contribution of the IRC7S allele to the outstanding behaviour of HS strains (i.e., improved response to oxidative stress conditions and higher tolerance to high copper levels); however, we also identified a set of sequence variants with significant co-occurrence patterns with the IRC7S allele, which can be co-contributing to the fitness and competitive advantages of HS strains in wine fermentations.
Asunto(s)
Proteínas de Saccharomyces cerevisiae , Vino , Alelos , Liasas de Carbono-Azufre/genética , Fermentación , Genómica , Saccharomyces cerevisiae/genética , Saccharomyces cerevisiae/metabolismo , Proteínas de Saccharomyces cerevisiae/genética , Proteínas de Saccharomyces cerevisiae/metabolismo , Vino/análisisRESUMEN
Phaffia is an orange-colored basidiomycetous yeast genus of the order Cystofilobasidiales that contains a single species, P. rhodozyma. This species is the only fungus known to produce the economically relevant carotenoid astaxanthin. Although Phaffia was originally found in the Northern hemisphere, its diversity in the southern part of the globe has been shown to be much greater. Here we analyze the genomes of two Australasian lineages that are markedly distinct from P. rhodozyma. The two divergent lineages were investigated within a comprehensive phylogenomic study of representatives of the Cystofilobasidiales that supported the recognition of two novel Phaffia species, for which we propose the names of P. australis sp. nov. and P. tasmanica sp. nov. Comparative genomics and other analyses confirmed that the two new species have the typical Phaffia hallmark-the six genes necessary for the biosynthesis of astaxanthin could be retrieved from the draft genome sequences, and this carotenoid was detected in culture extracts. In addition, the organization of the mating-type (MAT) loci is similar to that of P. rhodozyma, with synteny throughout most regions. Moreover, cases of trans-specific polymorphism involving pheromone receptor genes and pheromone precursor proteins in the three Phaffia species, together with their shared homothallism, provide additional support for their classification in a single genus.
RESUMEN
This study uses population genomic data to estimate demographic and selection parameters in two sister lineages of the wild yeast Saccharomyces paradoxus and compare their evolution. We first estimate nucleotide and recombinational diversities in each of the two lineages to infer their population size and frequency of sex and then analyze the rate of mutation accumulation since divergence from their inferred common ancestor to estimate the generation time and efficacy of selection. We find that one of the lineages has significantly higher silent nucleotide diversity and lower linkage disequilibrium, indicating a larger population with more frequent sexual generations. The same lineage also shows shorter generation time and higher efficacy of purifying selection, the latter consistent with the finding of larger population size and more frequent sex. Similar analyses are also performed on the ancestries of individual strains within lineages and we find significant differences between strains implying variation in rates of mitotic cell divisions. Our sample includes some strains originating in the Chernobyl nuclear-accident exclusion zone, which has been subjected to high levels of radiation for nearly 30 years now. We find no evidence, however, for increased rates of mutation. Finally, there is a positive correlation between rates of mutation accumulation and length of growing period, as measured by latitude of the place of origin of strains. Our study illustrates the power of genomic analyses in estimating population and life history parameters and testing predictions based on population genetic theory.
Asunto(s)
Genoma Fúngico , Acumulación de Mutaciones , Saccharomyces/genética , Selección Genética , Aptitud Genética , Variación Genética , Recombinación Genética , Saccharomyces/efectos de la radiaciónRESUMEN
Saccharomyces cerevisiae-the most emblematic and industrially relevant yeast-has a long list of taxonomical synonyms. Formerly considered as distinct species, some of the synonyms represent variants with important industrial implications, like Saccharomyces boulardii or Saccharomyces diastaticus, but with an unclear status, especially among the fermentation industry, the biotechnology community and biologists not informed on taxonomic matters. Here, we use genomics to investigate a group of 45 reference strains (type strains) of former Saccharomyces species that are currently regarded as conspecific with S. cerevisiae. We show that these variants are distributed across the phylogenetic spectrum of domesticated lineages of S. cerevisiae, with emphasis on the most relevant technological groups, but absent in wild lineages. We analyzed the phylogeny of a representative and well-balanced dataset of S. cerevisiae genomes that deepened our current ecological and biogeographic assessment of wild populations and allowed the distinction, among wild populations, of those associated with low- or high-sugar natural environments. Some wild lineages from China were merged with wild lineages from other regions in Asia and in the New World, thus giving more resolution to the current model of expansion from Asia to the rest of the world. We reassessed several key domestication markers among the different domesticated populations. In some cases, we could trace their origin to wild reservoirs, while in other cases gene inactivation associated with domestication was also found in wild populations, thus suggesting that natural adaptation to sugar-rich environments predated domestication.
RESUMEN
A cryophilic basidiomycetous yeast unable to grow at 18 °C or higher temperatures was isolated from a subsurface permafrost layer collected in the Eastern Swiss Alps and from melted sea ice collected in the Artic at Frobisher Bay, Nunavut, Canada. Phylogenetic analyses employing combined sequences of the D1/D2 domain and ITS region indicated that the two new isolates belong to the family Camptobasidiaceae of the class Microbotryomycetes but are distantly related to any of the currently recognized species and genera. Consequently, the novel genus Cryolevonia, and the novel species Cryolevonia schafbergensis (type strain PYCC 8347T=CBS 16055T) are proposed to accommodate this cryophilic yeast. Although sparse hyphae and teliospore-like stuctures were observed upon prolonged incubation, a sexual cycle was not observed and therefore C. schafbergensis is documented solely from its asexual stage.
Asunto(s)
Basidiomycota/clasificación , Cubierta de Hielo/microbiología , Hielos Perennes/microbiología , Filogenia , Basidiomycota/aislamiento & purificación , Canadá , ADN de Hongos/genética , ADN Espaciador Ribosómico/genética , Técnicas de Tipificación Micológica , Análisis de Secuencia de ADN , SuizaRESUMEN
The Wickerhamiella and Starmerella genera form a clade (W/S clade) that branches close to Yarrowia lipolytica in the Saccharomycotina species tree. It comprises approximately 90 recognized species and 50 putative new species not formally described yet. The large majority of the members of the W/S clade are ecologically associated with flowers and floricolous insects. Many species exhibit unusual metabolic traits, like fructophily and the production of sophorolipids, which are glycolipids that can be used as environmentally friendly biosurfactants. Genomic data have not only firmly established the W/S clade but have also revealed a tumultuous evolution of metabolism marked by losses and gains of important metabolic pathways, among which alcoholic fermentation. Possibly the most surprising finding brought to light by comparative genomics concerned the large number of genes acquired by some species of the W/S clade from bacteria through horizontal gene transfer, many of which were shown to be functional in their new setting. This was facilitated by the genetic tractability of one species in the clade, Starmerella bombicola, which is used for the industrial production of sophorolipids. We suggest that high-density coverage of genome sequencing in this clade, combined with the possibility to conduct molecular genetics experiments in at least one species, has the potential to set the stage for yet more exciting discoveries concerning the evolution of yeast metabolism.