Publications by authors named "José Paulo Sampaio"

78 Publications

Nomenclatural issues concerning cultured yeasts and other fungi: why it is important to avoid unneeded name changes.

IMA Fungus 2021 Jul 13;12(1):18. Epub 2021 Jul 13.

Department of Microbiology, Meiji Pharmaceutical University, 2 Chome-522-1 Noshio, Kiyose, Tokyo, 204-8588, Japan.

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.
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http://dx.doi.org/10.1186/s43008-021-00067-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8278710PMC
July 2021

Global distribution of IRC7 alleles in Saccharomyces cerevisiae populations: a genomic and phenotypic survey within the wine clade.

Environ Microbiol 2021 Jun 11;23(6):3182-3195. Epub 2021 May 11.

Department of Genetics, Physiology and Microbiology. Unit of Microbiology. Biology Faculty, Complutense University of Madrid, Madrid, 28040, Spain.

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-β-lyase enzyme related volatile thiols production in wines, has two alleles: a full-length allele (IRC7 ) and a mutated one (IRC7 ), harbouring a 38 bp-deletion. Interestingly, IRC7 -encoding a less active enzyme - appears widespread amongst wine populations. Studying the global distribution of the IRC7 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 IRC7 -homozygous (HS) strains exhibited both fitness and competitive advantages compared with IRC7 -homozygous (HF) strains. There are some pieces of evidence of the direct contribution of the IRC7 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 IRC7 allele, which can be co-contributing to the fitness and competitive advantages of HS strains in wine fermentations.
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http://dx.doi.org/10.1111/1462-2920.15540DOI Listing
June 2021

The Untapped Australasian Diversity of Astaxanthin-Producing Yeasts with Biotechnological Potential- sp. nov. and sp. nov.

Microorganisms 2020 Oct 24;8(11). Epub 2020 Oct 24.

UCIBIO, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal.

is an orange-colored basidiomycetous yeast genus of the order Cystofilobasidiales that contains a single species, . This species is the only fungus known to produce the economically relevant carotenoid astaxanthin. Although 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 . The two divergent lineages were investigated within a comprehensive phylogenomic study of representatives of the Cystofilobasidiales that supported the recognition of two novel species, for which we propose the names of sp. nov. and sp. nov. Comparative genomics and other analyses confirmed that the two new species have the typical 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 () loci is similar to that of , with synteny throughout most regions. Moreover, cases of trans-specific polymorphism involving pheromone receptor genes and pheromone precursor proteins in the three species, together with their shared homothallism, provide additional support for their classification in a single genus.
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http://dx.doi.org/10.3390/microorganisms8111651DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7692969PMC
October 2020

Population Size, Sex and Purifying Selection: Comparative Genomics of Two Sister Taxa of the Wild Yeast Saccharomyces paradoxus.

Genome Biol Evol 2020 09;12(9):1636-1645

Department of Life Sciences, Imperial College London, Ascot, Berks, United Kingdom.

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.
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http://dx.doi.org/10.1093/gbe/evaa141DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7533043PMC
September 2020

Revisiting the Taxonomic Synonyms and Populations of -Phylogeny, Phenotypes, Ecology and Domestication.

Microorganisms 2020 Jun 15;8(6). Epub 2020 Jun 15.

UCIBIO, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal.

-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 or , 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 species that are currently regarded as conspecific with . We show that these variants are distributed across the phylogenetic spectrum of domesticated lineages of , 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 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.
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http://dx.doi.org/10.3390/microorganisms8060903DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7356373PMC
June 2020

The Wickerhamiella/Starmerella clade-A treasure trove for the study of the evolution of yeast metabolism.

Yeast 2020 04 26;37(4):313-320. Epub 2020 Feb 26.

Applied Molecular Biosciences Unit-UCIBIO, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

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.
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http://dx.doi.org/10.1002/yea.3463DOI Listing
April 2020

gen. nov. and sp. nov., a cryophilic yeast from ancient permafrost and melted sea ice.

Int J Syst Evol Microbiol 2020 Apr 5;70(4):2334-2338. Epub 2020 Feb 5.

UCIBIO, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

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 of the class but are distantly related to any of the currently recognized species and genera. Consequently, the novel genus , and the novel species (type strain PYCC 8347=CBS 16055) 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 is documented solely from its asexual stage.
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http://dx.doi.org/10.1099/ijsem.0.004040DOI Listing
April 2020

Yeast Diversity Associated with the Phylloplane of Corn Plants Cultivated in Thailand.

Microorganisms 2020 Jan 7;8(1). Epub 2020 Jan 7.

Department of Microbiology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand.

The ecology and diversity of phylloplane yeasts is less well understood in tropical regions than in temperate ones. Therefore, we investigated the yeast diversity associated with the phylloplane of corn, an economically important crop in Thailand, by a culture-dependent method. Thirty-six leaf samples were collected and 217 yeast strains were isolated by plating leaf-washings. The strains were grouped by PCR-fingerprinting and representative strains were identified by analysis of the D1/D2 domain of the large subunit rRNA gene. In total, 212 strains were identified within 10 species in the Ascomycota and 32 species in the Basidiomycota. Five strains represented potential new species in the Basidiomycota, one strain was recently described as and four strains belonged to the genera and . A higher number of strains in the Basidiomycota (81.6%) was obtained. was the species with the highest occurrence. Principal coordinates analysis ordinations of yeast communities revealed that there were no differences in the similarity of the sampling sites. The estimation of the expected species richness showed that the observed species richness was lower than expected. This work indicated that a majority of yeast associated with the phylloplane of corn plant belongs to the phylum Basidiomycota.
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http://dx.doi.org/10.3390/microorganisms8010080DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7022409PMC
January 2020

sp. nov., sp. nov. and sp. nov., three novel basidiomycetous yeast species isolated from crater lakes.

Int J Syst Evol Microbiol 2019 Dec;69(12):3728-3739

China General Microbiological Culture Collection Center and State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, PR China.

The Arxan-Chaihe volcanic field of the Da Hinggan mountains in north-East PR China hosts various typical crater lakes. In this study we performed a yeast diversity survey using water sampled from five crater lakes and a total of 122 yeast strains belonging to 33 species of 25 genera were isolated. Three strains, TFL1-L, TFL2B and ATC4C, were identified as three novel species belonging to the based on a multiple gene phylogeny and on the comparison of physiological data. A phylogenetic study employing the sequences of seven genes indicated that the new species were more related to three separated phylogenetic lineages of the and their closest relatives were , and . The divergence values of the D1/D2 domain of LSU sequences of strains TFL1-L, TFL2B and ATC4C from CBS 8678, CBS 5029 and SN-82 were 4.8,3.4,2.1 %, respectively. The divergence values of the sequences of ITS regions between strains TFL1-L, TFL2B and ATC4C and their close relatives (, and ) were 16.1, 5.9 and 8.1  %, respectively. Moreover, the three strains differed from their phylogenetic neighbours by the ability to grow on distinct carbon and nitrogen sources. On the basis of these findings, it is suggested that these strains represent three novel species for which the names sp. nov. (holotype CGMCC 2.5595), sp. nov. (holotype CGMCC 2.5580) and sp. nov. (holotype CGMCC 2.5574) are proposed.
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http://dx.doi.org/10.1099/ijsem.0.003637DOI Listing
December 2019

Fermentation innovation through complex hybridization of wild and domesticated yeasts.

Nat Ecol Evol 2019 11 21;3(11):1576-1586. Epub 2019 Oct 21.

Laboratory of Genetics, J. F. Crow Institute for the Study of Evolution, Wisconsin Energy Institute, Genome Center of Wisconsin, University of Wisconsin-Madison, Madison, WI, USA.

The most common fermented beverage, lager beer, is produced by interspecies hybrids of the brewing yeast Saccharomyces cerevisiae and its wild relative S. eubayanus. Lager-brewing yeasts are not the only example of hybrid vigour or heterosis in yeasts, but the full breadth of interspecies hybrids associated with human fermentations has received less attention. Here we present a comprehensive genomic analysis of 122 Saccharomyces hybrids and introgressed strains. These strains arose from hybridization events between two to four species. Hybrids with S. cerevisiae contributions originated from three lineages of domesticated S. cerevisiae, including the major wine-making lineage and two distinct brewing lineages. In contrast, the undomesticated parents of these interspecies hybrids were all from wild Holarctic or European lineages. Most hybrids have inherited a mitochondrial genome from a parent other than S. cerevisiae, which recent functional studies suggest could confer adaptation to colder temperatures. A subset of hybrids associated with crisp flavour profiles, including both lineages of lager-brewing yeasts, have inherited inactivated S. cerevisiae alleles of critical phenolic off-flavour genes and/or lost functional copies from the wild parent through multiple genetic mechanisms. These complex hybrids shed light on the convergent and divergent evolutionary trajectories of interspecies hybrids and their impact on innovation in lager brewing and other diverse fermentation industries.
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http://dx.doi.org/10.1038/s41559-019-0998-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7295394PMC
November 2019

sp. nov. and sp. nov., two novel basidiomycetous yeast species isolated from grape and apple must in Italy.

Int J Syst Evol Microbiol 2019 Nov;69(11):3385-3391

PYCC - Portuguese Yeast Culture Collection, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

During a survey of yeast populations associated with grape and apple musts used for wine and cider fermentation, respectively, six pink-coloured ballistoconidia-forming yeasts belonging to the order (Basidiomycota) were isolated. Phylogenetic analysis inferred using sequences of the internal transcribed spacer (ITS), the D1/D2 domain of the large subunit rRNA gene, the small subunit (SSU) rRNA gene and DNA-directed RNA polymerase II subunit () indicated that the six isolates were separated in two novel species. One of the new species, sp. nov., isolated from grape must, had and as its closest relatives, but showed four/two and 16 nucleotide substitutions in the D1/D2 and ITS regions, respectively, to these two species. The other novel species, sp. nov., was found in apple must and was closely related to and , but showed two/three and five substitutions in those two regions for its closest relatives. We detected additional representatives of this species, most of them isolated from grapes whose sequences were already available on public databases. A sexual stage could not be observed for the novel species.
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http://dx.doi.org/10.1099/ijsem.0.003626DOI Listing
November 2019

A Quasi-Domesticate Relic Hybrid Population of × Adapted to Olive Brine.

Front Genet 2019 29;10:449. Epub 2019 May 29.

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

The adaptation of the yeast to man-made environments for the fermentation of foodstuffs and beverages illustrates the scientific, social, and economic relevance of microbe domestication. Here we address a yet unexplored aspect of domestication, that of the emergence of lineages harboring some domestication signatures but that do not fit completely in the archetype of a domesticated yeast, by studying strains associated with processed olives, namely table olives, olive brine, olive oil, and alpechin. We confirmed earlier observations that reported that the Olives population results from a hybridization between and We concluded that the olive hybrids form a monophyletic lineage and that the progenitor belonged to the wine population of this species. We propose that homoploid hybridization gave rise to a diploid hybrid genome, which subsequently underwent the loss of most of the sub-genome. Such a massive loss of heterozygosity was probably driven by adaptation to the new niche. We observed that olive strains are more fit to grow and survive in olive brine than control wine strains and that they appear to be adapted to cope with the presence of NaCl in olive brine through expansion of copy number of genes. We also investigated whether the HXT alleles retained by the Olives population were likely to contribute to the observed superior ability of these strains to consume sugars in brine. Our experiments indicate that sugar consumption profiles in the presence of NaCl are different between members of the Olives and Wine populations and only when cells are cultivated in nutritional conditions that support adaptation of their proteome to the high salt environment, which suggests that the observed differences are due to a better overall fitness of olives strains in the presence of high NaCl concentrations. Although relic olive hybrids exhibit several characteristics of a domesticated lineage, tangible benefits to humans cannot be associated with their phenotypes. These strains can be seen as a case of adaptation without positive or negative consequences to humans, that we define as a quasi-domestication.
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http://dx.doi.org/10.3389/fgene.2019.00449DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6548830PMC
May 2019

Microbe Profile: Saccharomyces eubayanus, the missing link to lager beer yeasts.

Microbiology (Reading) 2018 09;164(9):1069-1071

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal.

Saccharomyces eubayanus was described less than 10 years ago and its discovery settled the long-lasting debate on the origins of the cold-tolerant yeast responsible for lager beer fermentation. The largest share of the genetic diversity of S. eubayanus is located in South America, and strains of this species have not yet been found in Europe. One or more hybridization events between S. eubayanus and S. cerevisiae ale beer strains gave rise to S. pastorianus, the allopolyploid yeasts responsible for lager beer production worldwide. The identification of the missing progenitor of lager yeast opened new avenues for brewing yeast research. It allowed not only the selective breeding of new lager strains, but revealed also a wild yeast with interesting brewing abilities so that a beer solely fermented by S. eubayanus is currently on the market.
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http://dx.doi.org/10.1099/mic.0.000677DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6230766PMC
September 2018

Multiple Rounds of Artificial Selection Promote Microbe Secondary Domestication-The Case of Cachaça Yeasts.

Genome Biol Evol 2018 08 1;10(8):1939-1955. Epub 2018 Aug 1.

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

The study of microbe domestication has witnessed major advances that contribute to a better understanding of the emergence of artificially selected phenotypes and set the foundations of their rational improvement for biotechnology. Several features make Saccharomyces cerevisiae an ideal model for such a study, notably the availability of a catalogue of signatures of artificial selection and the extensive knowledge available on its biological processes. Here, we investigate with population and comparative genomics a set of strains used for cachaça fermentation, a Brazilian beverage based on the fermentation of sugar cane juice. We ask if the selective pressures posed by this fermentation have given rise to a domesticated lineage distinct from the ones already known, like wine, beer, bread, and sake yeasts. Our results show that cachaça yeasts derive from wine yeasts that have undergone an additional round of domestication, which we define as secondary domestication. As a consequence, cachaça strains combine features of wine yeasts, such as the presence of genes relevant for wine fermentation and advantageous gene inactivations, with features of beer yeasts like resistance to the effects of inhibitory compounds present in molasses. For other markers like those related to sulfite resistance and biotin metabolism our analyses revealed distributions more complex than previously reported that support the secondary domestication hypothesis. We propose a multilayered microbe domestication model encompassing not only transitions from wild to primarily domesticated populations, as in the case of wine yeasts, but also secondary domestications like those of cachaça yeasts.
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http://dx.doi.org/10.1093/gbe/evy132DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6101510PMC
August 2018

Blastobotrys bombycis sp. nov., a d-xylose-fermenting yeast isolated from the gut of the silkworm larva Bombyx mori.

Int J Syst Evol Microbiol 2018 Aug 27;68(8):2638-2643. Epub 2018 Jun 27.

2​National Fungal Culture Collection of India (NFCCI), Biodiversity and Palaeobiology Group, MACS-Agharkar Research Institute, G.G. Agarkar Road, Pune 411004, India.

The gut of insects harbors a yeast community that is still poorly understood. Here, a novel species of the ascomycetous genus Blastobotrys is proposed based on a yeast strain isolated from the larval gut of the silkworm Bombyx mori (Order Lepidoptera). The novel species is closely related to Blastobotrys aristata and Blastobotrys elegans on the basis of the results of molecular phylogenetic analyses. A preliminary screening revealed that it produces 1.5 g l ethanol by fermenting 5 % d-xylose. The novel species, that represents the first report, to our knowledge, of yeast isolation from silkworms, is described as Blastobotrys bombycis sp. nov. (type strain RAAB001=CBS 15274=PYCC 8105=MCC 1427; MycoBank accession number MB 825095).
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http://dx.doi.org/10.1099/ijsem.0.002890DOI Listing
August 2018

Zygotorulaspora chibaensis sp. nov. and Zygotorulaspora danielsina sp. nov., novel ascomycetous yeast species from tree bark and soil.

Int J Syst Evol Microbiol 2018 Aug 22;68(8):2633-2637. Epub 2018 Jun 22.

1​UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

Multiple isolates belonging to the ascomycetous genus Zygotorulaspora were obtained from forest soils and tree bark in Shiba Prefecture in Japan, and Lake Daniels, Lewis Pass, in New Zealand. Phylogenetic analyses employing combined sequences of the D1/D2 domain and ITS region support the recognition of two new species: Zygotorulaspora chibaensis sp. nov. (type strain PYCC 6970=CBS 15364) and Zygotorulaspora danielsina sp. nov. (type strain PYCC 6984=CBS 15365). Both species are able to grow on d-xylose and l-arabinose and at 35 °C, unlike Zygotorulaspora florentina and Zygotorulaspora mrakii, the other two species in the genus.
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http://dx.doi.org/10.1099/ijsem.0.002889DOI Listing
August 2018

Occultifur mephitis f.a., sp. nov. and other yeast species from hypoxic and elevated CO2 mofette environments.

Int J Syst Evol Microbiol 2018 Jul 29;68(7):2285-2298. Epub 2018 May 29.

Department of Agronomy, Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia.

An inventory of culturable yeasts from the soil and water of natural CO2 springs (mofettes) in northeast Slovenia is presented. In mofettes, CO2 of geological origin reaches the soil surface causing temporarily and spatially stable hypoxic environments in soil and water. In total, 142 yeast strains were isolated and identified from high CO2 and control meadow soil, meadow ground-water, forest pond and stream water. All water locations showed below-ground CO2 release. They were assigned to six basidiomycetous yeast genera (six species) and 11 ascomycetous genera (18 species). All ascomycetous yeasts, with the exception of Debaryomyces hansenii, were able to grow under elevated CO2 and fermented glucose. Candida sophiae-reginae, Pichia fermentans and Candida vartiovaarae were the dominating species in meadow and forest high CO2 exposed water. Meyerozyma guilliermondii and Wickerhamomyces anomalus predominated in high CO2 exposed soils. Using high dilution plating of a mofette soil sample, four strains of an unknown basidiomycetous species were isolated and are here newly described as Occultifur mephitis based on molecular phylogenetic and phenotypic criteria. The type strain of Occultifur mephitis is EXF-6436[CBS 14611=PYCC 7049, LT594852 (D1/D2), KX929055 (ITS)]. An additional three isolated strains are EXF-6437 (LT594853, KX929056), EXF-6473 (LT594863, KX929057) and EXF-6482 (LT594867, KX929054), as well as a strain reported from previous studies isolated from a leaf of Cistus albidus in Portugal (CBS 10223=PYCC 6067), EU002842 (D1/D2), KY308183 (ITS).
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http://dx.doi.org/10.1099/ijsem.0.002824DOI Listing
July 2018

Adaptation of S. cerevisiae to Fermented Food Environments Reveals Remarkable Genome Plasticity and the Footprints of Domestication.

Mol Biol Evol 2018 07;35(7):1712-1727

SPO, Univ Montpellier, INRA, Montpellier SupAgro, Montpellier, France.

The budding yeast Saccharomyces cerevisiae can be found in the wild and is also frequently associated with human activities. Despite recent insights into the phylogeny of this species, much is still unknown about how evolutionary processes related to anthropogenic niches have shaped the genomes and phenotypes of S. cerevisiae. To address this question, we performed population-level sequencing of 82 S. cerevisiae strains from wine, flor, rum, dairy products, bakeries, and the natural environment (oak trees). These genomic data enabled us to delineate specific genetic groups corresponding to the different ecological niches and revealed high genome content variation across the groups. Most of these strains, compared with the reference genome, possessed additional genetic elements acquired by introgression or horizontal transfer, several of which were population-specific. In addition, several genomic regions in each population showed evidence of nonneutral evolution, as shown by high differentiation, or of selective sweeps including genes with key functions in these environments (e.g., amino acid transport for wine yeast). Linking genetics to lifestyle differences and metabolite traits has enabled us to elucidate the genetic basis of several niche-specific population traits, such as growth on galactose for cheese strains. These data indicate that yeast has been subjected to various divergent selective pressures depending on its niche, requiring the development of customized genomes for better survival in these environments. These striking genome dynamics associated with local adaptation and domestication reveal the remarkable plasticity of the S. cerevisiae genome, revealing this species to be an amazing complex of specialized populations.
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http://dx.doi.org/10.1093/molbev/msy066DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5995190PMC
July 2018

sp. nov. and sp. nov. from European Cold Environments and Arctic Region.

Life (Basel) 2018 May 5;8(2). Epub 2018 May 5.

Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, SI-1000 Ljubljana, Slovenia.

Over 80% of the Earth’s environments are permanently or periodically exposed to temperatures below 5 °C. Cold habitats harbour a wide diversity of psychrophilic and psychrotolerant yeasts. During ecological studies of yeast communities carried out in cold ecosystem in the Italian Alps, Svalbard (Norway, Arctic region), and Portugal, 23 yeast strains that could not be assigned to any known fungal taxa were isolated. In particular, two of them were first identified as sp., showing the highest degree of D1/D2 sequence identity with accounted to only 97% with the type strain ( CBS 2221). The other 21 strains, exhibiting identical D1/D2 sequences, had low identity (97%) with and . Similarly, ITS sequences of the type strains of the most closely related species (93⁻94%). In a 2-genes multilocus D1/D2 and ITS ML phylogenetic tree, the studied strains pooled in two well separated and supported groups. In order to classify the new 23 isolates based on phylogenetic evidences, we propose the description of two novel species sp. nov. and sp. nov.
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http://dx.doi.org/10.3390/life8020009DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6027198PMC
May 2018

Papiliotrema plantarum sp. nov., a novel tremellaceous sexual yeast species.

Int J Syst Evol Microbiol 2018 Jun 20;68(6):1937-1941. Epub 2018 Apr 20.

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

During a survey of the yeast community associated with the phylloplane of corn in Thailand, a basidiomycetous yeast strain belonging to the genus Papiliotrema was isolated. Analyses of the D1/D2 domains of the 26S (LSU) rRNA gene and complete ITS region supported the recognition of a novel species, for which the name Papiliotrema plantarum sp. nov. is proposed (type strain DMKU-CP801=CBS 15220=PYCC 7257). Another strain of P. plantarum sp. nov., isolated in French Guiana, was found to be sexually compatible with the Thai isolate and mycelium with clamp connections, basidia and basidiospores were observed in culture. The basidial morphology of P. plantarum combined features previously observed for Papiliotrema bandonii and Papiliotrema fuscus, which represent the only sexual species hitherto known in the genus, i.e. transversely septate basidia, with sexual structures of the Tremella type.
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http://dx.doi.org/10.1099/ijsem.0.002771DOI Listing
June 2018

Taxonomic annotation of public fungal ITS sequences from the built environment - a report from an April 10-11, 2017 workshop (Aberdeen, UK).

MycoKeys 2018 8(28):65-82. Epub 2018 Jan 8.

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Inhoffenstrasse 7 B, 38124 Braunschweig, Germany.

Recent DNA-based studies have shown that the built environment is surprisingly rich in fungi. These indoor fungi - whether transient visitors or more persistent residents - may hold clues to the rising levels of human allergies and other medical and building-related health problems observed globally. The taxonomic identity of these fungi is crucial in such pursuits. Molecular identification of the built mycobiome is no trivial undertaking, however, given the large number of unidentified, misidentified, and technically compromised fungal sequences in public sequence databases. In addition, the sequence metadata required to make informed taxonomic decisions - such as country and host/substrate of collection - are often lacking even from reference and ex-type sequences. Here we report on a taxonomic annotation workshop (April 10-11, 2017) organized at the James Hutton Institute/University of Aberdeen (UK) to facilitate reproducible studies of the built mycobiome. The 32 participants went through public fungal ITS barcode sequences related to the built mycobiome for taxonomic and nomenclatural correctness, technical quality, and metadata availability. A total of 19,508 changes - including 4,783 name changes, 14,121 metadata annotations, and the removal of 99 technically compromised sequences - were implemented in the UNITE database for molecular identification of fungi (https://unite.ut.ee/) and shared with a range of other databases and downstream resources. Among the genera that saw the largest number of changes were , , , and , all of them of significant importance in both culture-based and culture-independent surveys of the built environment.
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http://dx.doi.org/10.3897/mycokeys.28.20887DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5804120PMC
January 2018

Moniliella sojae sp. nov., a species of black yeasts isolated from Vietnamese soy paste (tuong), and reassignment of Moniliella suaveolens strains to Moniliella pyrgileucina sp. nov., Moniliella casei sp. nov. and Moniliella macrospora emend. comb. nov.

Int J Syst Evol Microbiol 2018 May 9;68(5):1806-1814. Epub 2018 Mar 9.

Department of Biology, University of Western Ontario, London, ON N6A 5B7, Canada.

The presence of yeasts at different steps of Vietnamese soy paste production was studied. Yeast growth occurred during primary soybean fermentation, with the cell density reaching 4.10 c.f.u. ml, and terminated during brine fermentation. The dominant species were Pichia kudriavzevii and Millerozyma farinosa. Over the span of 14 years, nine strains of Moniliella were isolated. The strains had identical PCR fingerprints generated with primer (GAC)5 and identical D1/D2 and internal transcribed spacer (ITS) sequences. A D1/D2-based phylogeny indicated that the strains were closest to a group of four previously assigned as Moniliella suaveolens strains. Together they form a new lineage that is well separated from all known species, including M. suaveolens (over 12.7 % divergence). ITS sequences indicated the presence of four species differing from each other by 9-57 nt. The name Moniliella sojae sp. nov. is proposed to accommodate the strains isolated from Vietnamese soy paste, Moniliella pyrgileucina sp. nov. is proposed for PYCC 6800 and Moniliella casei sp. nov. is proposed for CBS 157.58. An emended combination Moniliella macrospora is proposed for CBS 221.32 and CBS 223.32. The type strains and MycoBank numbers are: M. sojae sp. nov., SS 4.2=CBS 126448=NRRL Y-48680 and MB 822871; M. pyrgileucina sp. nov., PYCC 6800=CBS 15203 and MB 823030; M. casei sp. nov., CBS 157.58=IFM 60348 and MB 822872; M. macrospora emend. comb. nov., CBS 221.32 (=MUCL 11527) and MB 822874.
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http://dx.doi.org/10.1099/ijsem.0.002690DOI Listing
May 2018

Cryptotrichosporon argae sp. nov., Cryptotrichosporon brontae sp. nov. and Cryptotrichosporon steropae sp. nov., isolated from forest soils.

Int J Syst Evol Microbiol 2017 Sep 6;67(9):3610-3614. Epub 2017 Sep 6.

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

Yeast strains belonging to the basidiomycetous genus Cryptotrichosporon were isolated from forest soils in Serra da Arrábida Natural Park in Portugal. Similar to the already-known representatives of this genus, the new isolates formed pigmented colonies of a distinctive pale orange colour. Phylogenetic analyses employing concatenated sequences of the D1/D2 domains of the 26S (large subunit) rRNA gene and the internal transcribed spacer (ITS) region supported the recognition of three novel species: Cryptotrichosporon argae sp. nov. (type strain CM 19T=CBS 14376T=PYCC 7010T=DSM 104550T; MycoBank accession number MB 817168), Cryptotrichosporon brontae sp. nov. (type strain CM 1562T=CBS 14303T=PYCC 7011T=DSM 104551T; MycoBank accession number MB 817077) and Cryptotrichosporon steropae sp. nov. (type strain OR 395T=CBS 14302T=PYCC 7012T=DSM 104552T; MycoBank accession number MB 817078).
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http://dx.doi.org/10.1099/ijsem.0.002177DOI Listing
September 2017

Hybridization and adaptive evolution of diverse species for cellulosic biofuel production.

Biotechnol Biofuels 2017 27;10:78. Epub 2017 Mar 27.

Laboratory of Genetics, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, Genome Center of Wisconsin, University of Wisconsin-Madison, Madison, WI USA.

Background: Lignocellulosic biomass is a common resource across the globe, and its fermentation offers a promising option for generating renewable liquid transportation fuels. The deconstruction of lignocellulosic biomass releases sugars that can be fermented by microbes, but these processes also produce fermentation inhibitors, such as aromatic acids and aldehydes. Several research projects have investigated lignocellulosic biomass fermentation by the baker's yeast . Most projects have taken synthetic biological approaches or have explored naturally occurring diversity in to enhance stress tolerance, xylose consumption, or ethanol production. Despite these efforts, improved strains with new properties are needed. In other industrial processes, such as wine and beer fermentation, interspecies hybrids have combined important traits from multiple species, suggesting that interspecies hybridization may also offer potential for biofuel research.

Results: To investigate the efficacy of this approach for traits relevant to lignocellulosic biofuel production, we generated synthetic hybrids by crossing engineered xylose-fermenting strains of with wild strains from various species. These interspecies hybrids retained important parental traits, such as xylose consumption and stress tolerance, while displaying intermediate kinetic parameters and, in some cases, heterosis (hybrid vigor). Next, we exposed them to adaptive evolution in ammonia fiber expansion-pretreated corn stover hydrolysate and recovered strains with improved fermentative traits. Genome sequencing showed that the genomes of these evolved synthetic hybrids underwent rearrangements, duplications, and deletions. To determine whether the genus contains additional untapped potential, we screened a genetically diverse collection of more than 500 wild, non-engineered isolates and uncovered a wide range of capabilities for traits relevant to cellulosic biofuel production. Notably, strains have high innate tolerance to hydrolysate toxins, while some species have a robust native capacity to consume xylose.

Conclusions: This research demonstrates that hybridization is a viable method to combine industrially relevant traits from diverse yeast species and that members of the genus beyond may offer advantageous genes and traits of interest to the lignocellulosic biofuel industry.
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http://dx.doi.org/10.1186/s13068-017-0763-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5369230PMC
March 2017

Adaptive divergence in wine yeasts and their wild relatives suggests a prominent role for introgressions and rapid evolution at noncoding sites.

Mol Ecol 2017 Apr 22;26(7):2167-2182. Epub 2017 Mar 22.

Departamento de Ciências da Vida, UCIBIO-REQUIMTE, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516, Caparica, Portugal.

In Saccharomyces cerevisiae, the main yeast in wine fermentation, the opportunity to examine divergence at the molecular level between a domesticated lineage and its wild counterpart arose recently due to the identification of the closest relatives of wine strains, a wild population associated with Mediterranean oaks. As genomic data are available for a considerable number of representatives belonging to both groups, we used population genomics to estimate the degree and distribution of nucleotide variation between wine yeasts and their closest wild relatives. We found widespread genomewide divergence, particularly at noncoding sites, which, together with above average divergence in trans-acting DNA binding proteins, may suggest an important role for divergence at the level of transcriptional regulation. Nine outlier regions putatively under strong divergent selection were highlighted by a genomewide scan under stringent conditions. Several cases of introgressions, originating in the sibling species Saccharomyces paradoxus, were also identified in the Mediterranean oak population. FZF1 and SSU1, mostly known for conferring sulphite resistance in wine yeasts, were among the introgressed genes, although not fixed. Because the introgressions detected in our study are not found in wine strains, we hypothesize that ongoing divergent ecological selection segregates the two forms between the different niches. Together, our results provide a first insight into the extent and kind of divergence between wine yeasts and their closest wild relatives.
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http://dx.doi.org/10.1111/mec.14071DOI Listing
April 2017

Libkindia masarykiana gen. et sp. nov., Yurkovia mendeliana gen. et sp. nov. and Leucosporidium krtinense f.a. sp. nov., isolated from temperate forest soils.

Int J Syst Evol Microbiol 2017 Apr 5;67(4):902-908. Epub 2017 May 5.

Laboratory of Environmental Microbiology, Institute of Microbiology of the CAS, Vídeňská 1083, 14220 Praha 4, Czech Republic.

One hundred and ninety-eight isolates of soil yeasts were isolated from mixed temperate forests in the Czech Republic, and their abundance and distribution in the litter and soil were evaluated using amplicon sequencing of soil fungal communities. Abundant taxa with no close identified hits were selected for further characterization as potential novel species of yeasts. Phylogenetic analyses using sequences of the D1/D2 domain, the ITS region and RPB1 and TEF1 genes support the recognition of the following three novel species belonging to the subphylum Pucciniomycotina, class Microbotryomycetes: Leucosporidium krtinense f.a. sp. nov. (type strain PYCC 6879T=KT96T=CBS 14304T=DSM 101892T), Yurkovia mendeliana sp. nov. (type strain PYCC 6884T=KT152T=CBS 14273T=DSM 101889T) and Libkindia masarykiana sp. nov. (type strain PYCC 6886T=KT310T=CBS 14275T=DSM 101891T). Since the latter two novel taxa cannot be assigned to existing genera, two new genera, Libkindia gen. nov. and Yurkovia gen. nov., are also described.
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http://dx.doi.org/10.1099/ijsem.0.001707DOI Listing
April 2017

Distinct Domestication Trajectories in Top-Fermenting Beer Yeasts and Wine Yeasts.

Curr Biol 2016 10 6;26(20):2750-2761. Epub 2016 Oct 6.

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal. Electronic address:

Beer is one of the oldest alcoholic beverages and is produced by the fermentation of sugars derived from starches present in cereal grains. Contrary to lager beers, made by bottom-fermenting strains of Saccharomyces pastorianus, a hybrid yeast, ale beers are closer to the ancient beer type and are fermented by S. cerevisiae, a top-fermenting yeast. Here, we use population genomics to investigate (1) the closest relatives of top-fermenting beer yeasts; (2) whether top-fermenting yeasts represent an independent domestication event separate from those already described; (3) whether single or multiple beer yeast domestication events can be inferred; and (4) whether top-fermenting yeasts represent non-recombinant or recombinant lineages. Our results revealed that top-fermenting beer yeasts are polyphyletic, with a main clade composed of at least three subgroups, dominantly represented by the German, British, and wheat beer strains. Other beer strains were phylogenetically close to sake, wine, or bread yeasts. We detected genetic signatures of beer yeast domestication by investigating genes previously linked to brewing and using genome-wide scans. We propose that the emergence of the main clade of beer yeasts is related with a domestication event distinct from the previously known cases of wine and sake yeast domestication. The nucleotide diversity of the main beer clade more than doubled that of wine yeasts, which might be a consequence of fundamental differences in the modes of beer and wine yeast domestication. The higher diversity of beer strains could be due to the more intense and different selection regimes associated to brewing.
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http://dx.doi.org/10.1016/j.cub.2016.08.040DOI Listing
October 2016

Genetic Dissection of Sexual Reproduction in a Primary Homothallic Basidiomycete.

PLoS Genet 2016 06 21;12(6):e1006110. Epub 2016 Jun 21.

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.

In fungi belonging to the phylum Basidiomycota, sexual compatibility is usually determined by two genetically unlinked MAT loci, one of which encodes one or more pheromone receptors (P/R) and pheromone precursors, and the other comprehends at least one pair of divergently transcribed genes encoding homeodomain (HD) transcription factors. Most species are heterothallic, meaning that sexual reproduction requires mating between two sexually compatible individuals harboring different alleles at both MAT loci. However, some species are known to be homothallic, one individual being capable of completing the sexual cycle without mating with a genetically distinct partner. While the molecular underpinnings of the heterothallic life cycles of several basidiomycete model species have been dissected in great detail, much less is known concerning the molecular basis for homothallism. Following the discovery in available draft genomes of the homothallic basidiomycetous yeast Phaffia rhodozyma of P/R and HD genes, we employed available genetic tools to determine their role in sexual development. Two P/R clusters, each harboring one pheromone receptor and one pheromone precursor gene were found in close vicinity of each other and were shown to form two redundant P/R pairs, each receptor being activated by the pheromone encoded by the most distal pheromone precursor gene. The HD locus is apparently genetically unlinked to the P/R locus and encodes a single pair of divergently transcribed HD1 and HD2 transcription factors, both required for normal completion of the sexual cycle. Given the genetic makeup of P. rhodozyma MAT loci, we postulate that it is a primarily homothallic organism and we propose a model for the interplay of molecular interactions required for sexual development in this species. Phaffia rhodozyma is considered one of the most promising microbial source of the carotenoid astaxanthin. Further development of this yeast as an industrial organism will benefit from new insights regarding its sexual reproduction system.
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http://dx.doi.org/10.1371/journal.pgen.1006110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915694PMC
June 2016

Yamadazyma barbieri f.a. sp. nov., an ascomycetous anamorphic yeast isolated from a Mid-Atlantic Ridge hydrothermal site (-2300 m) and marine coastal waters.

Int J Syst Evol Microbiol 2016 Sep 14;66(9):3600-3606. Epub 2016 Jun 14.

Micalis Institute, INRA, AgroParisTech, CIRM-Levures, Université Paris-Saclay, 78350 Jouy-en-Josas, France.

Two yeast strains that are members of the same species were isolated from different marine habitats, i.e. one from Mid-Atlantic Ridge ocean water samples located in the direct vicinity of black smokers near the Rainbow deep-sea hydrothermal vent and one from Brazilian marine water samples off the Ipanema beach. Strains CLIB 1964T and CLIB 1965 are anamorphic ascomycetous yeasts affiliated to the Yamadazyma clade of Saccharomycetales. Interestingly, these strains were phylogenetically and distinctly positioned into a group of species comprising all species of the genus Yamadazyma isolated from marine habitats including deep-sea hydrothermal vents, i.e.Candida atmosphaerica,C. spencermartinsiae,C. atlantica,C. oceani and C. taylorii. These strains differed significantly in their D1/D2 domain sequences of the LSU rRNA gene from the closely related species mentioned above, by 2.6, 3.0, 3.4, 3.8 and 6.0 %, respectively. Internal transcribed spacer region sequence divergence was also significant and corresponded to 4.6, 4.7, 4.7, 12.0 and 24.7 % with C. atlantica,C. atmosphaerica, C. spencermartinsiae,C. oceani and C. taylorii, respectively. Phenotypically, strains CLIB 1964T and CLIB 1965 could be distinguished from closely related species by their inability to assimilate l-sorbose. CLIB 1964T (=CBS 14301T=UBOCC-A-214001T) is the designated type strain for Yamadazyma barbieri sp. nov. The MycoBank number is MB 815884.
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http://dx.doi.org/10.1099/ijsem.0.001239DOI Listing
September 2016

Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae.

Genome Biol Evol 2016 Jan 18;8(2):317-29. Epub 2016 Jan 18.

UCIBIO-REQUIMTE, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal

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, a tropical 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.
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http://dx.doi.org/10.1093/gbe/evv263DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4779607PMC
January 2016