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Bensasson, D.

Publications and source records attributed to Bensasson, D..

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Low level contamination confounds population genomic analysis

Genome sequence contamination has a variety of causes and can originate from within or between species. Previous research focused primarily on cross-species contamination or on prokaryotes. This paper visualizes B-allele frequency to test for intra-species contamination, and measures its effects on phylogenetic and admixture analysis in two fungal species. Using a standard base calling pipeline, we found that contaminated genomes superficially appeared to produce good quality genome data. Yet as little as 5-10% genome contamination was enough to change phylogenetic tree topologies and make contaminated strains appear as hybrids between lineages (genetically admixed). We recommend the use of B-allele frequency plots to screen genome resequencing data for intra-species contamination.

genomics↗

Footprints of human migration in the population structure of wild wine yeast

Humans have a long history of fermenting food and beverages that led to domestication of the wine yeast, Saccharomyces cerevisiae. Despite their tight companionship with humans, yeast species that are domesticated or pathogenic can also live on trees. Here we used over 300 genomes of S. cerevisiae from oaks and other trees to determine whether tree-associated populations are genetically distinct from domesticated lineages and estimate the timing of forest lineage divergence. We found populations on trees are highly structured within Europe, Japan, and North America. Approximate estimates of when forest lineages diverged out of Asia and into North America and Europe coincide with the end of the last ice age, the spread of agriculture, and the onset of fermentation by humans. It appears that migration from human-associated environments to trees is ongoing. Indeed, patterns of ancestry in the genomes of three recent migrants from the trees of North America to Europe could be explained by the human response to the Great French Wine Blight. Our results suggest that human-assisted migration affects forest populations, albeit rarely. Such migration events may even have shaped the global distribution of S. cerevisiae. Given the potential for lasting impacts due to yeast migration between human and natural environments, it seems important to understand the evolution of human commensals and pathogens in wild niches.

evolutionary biology↗

Genetic variation in aneuploidy prevalence and tolerance across the Saccharomyces cerevisiae phylogeny

Individuals carrying an aberrant number of chromosomes can vary widely in their expression of aneuploidy phenotypes. A major unanswered question is the degree to which an individuals genetic makeup influences its tolerance of karyotypic imbalance. Here we took a population genetics perspective to investigate the selective forces influencing aneuploidy prevalence in Saccharomyces cerevisiae populations as a model for eukaryotic biology. We analyzed genotypic and phenotypic variation recently published for over 1,000 S. cerevisiae strains spanning dozens of genetically defined clades and ecological associations. Our results show that the prevalence of chromosome gain and loss varies by clade and can be better explained by differences in genetic background than ecology. The phylogenetic context of lineages showing high aneuploidy rates suggests that increased aneuploidy frequency arose multiple times in S. cerevisiae evolution. Separate from aneuploidy frequency, analyzing growth phenotypes reveals that some backgrounds - such as European Wine strains - show fitness costs upon chromosome duplication, whereas other clades with high aneuploidy rates show little evidence of major deleterious effects. Our analysis confirms that chromosome amplification can produce phenotypic benefits that can influence evolutionary trajectories. These results have important implications for understanding genetic variation in aneuploidy prevalence in health, disease, and evolution. ARTICLE SUMMARYAneuploidy, an imbalance in the normal chromosome copy number, is detrimental during human development; yet individuals show substantial variability in their aneuploidy susceptibility, suggesting the influence of genetic background on aneuploidy tolerance. Scopel et al. employed a population genetic approach to address this question, analyzing over 1,000 published Saccharomyces cerevisiae genomes. The results demonstrate that genetic background has a substantial effect on aneuploidy frequency and cellular tolerance of aneuploidy stress, presenting important new information on the forces that contribute to aneuploidy prevalence.

genetics↗

Evolution of Ty1 copy number control in yeast by horizontal transfer of a gag gene

Insertion of mobile DNA sequences typically has deleterious effects on host fitness, and thus diverse mechanisms have evolved to control mobile element proliferation across the tree of life. Mobility of the Ty1 retrotransposon in Saccharomyces yeasts is regulated by a novel form of copy number control (CNC) mediated by a self-encoded restriction factor derived from the Ty1 gag capsid gene that inhibits virus-like particle function. Here, we survey a panel of wild and human-associated strains of S. cerevisiae and S. paradoxus to investigate how genomic Ty1 content influences variation in Ty1 mobility. We observe high levels of mobility for a canonical Ty1 tester element in permissive strains that either lack full-length Ty1 elements or only contain full-length copies of the Ty1 subfamily that have a divergent gag sequence. In contrast, low levels of canonical Ty1 mobility are observed in restrictive strains carrying full-length Ty1 elements containing canonical gag. Phylogenomic analysis of full-length Ty1 elements revealed that Ty1 is the ancestral subfamily present in wild strains of S. cerevisiae, and that canonical Ty1 in S. cerevisiae is a derived subfamily that acquired gag from S. paradoxus by horizontal transfer and recombination. Our results provide evidence that variation in the ability of S. cerevisiae and S. paradoxus strains to repress canonical Ty1 transposition via CNC is encoded by the genomic content of different Ty1 subfamilies, and that self-encoded forms of transposon control can spread across species boundaries by horizontal transfer.

evolutionary biology↗

Phased diploid genome assemblies for three strains of Candida albicans from oak trees

Although normally a harmless commensal, Candida albicans has the potential to generate a wide range of infections including systemic candidaemia, making it the most common cause of bloodstream infections worldwide with a high rate of mortality. C. albicans has long been considered an obligate commensal, however, recent studies suggest it can live outside animal hosts. Here, we have generated PacBio sequencing and phased genome assemblies for three C. albicans strains from oak trees in the United Kingdom (NCYC 4144, NCYC 4145, and NCYC 4146). Our results provide phased de novo diploid assemblies for C. albicans and provide a framework to study patterns of genomic variation within and among strains of an important fungal pathogen.

genomics↗

Diverse lineages of Candida albicans live on old oaks

The human pathogen, Candida albicans, is considered an obligate commensal of animals, yet it is occasionally isolated from trees, shrubs and grass. We generated deep genome sequence data for three strains of C. albicans that we isolated from oak trees in an ancient wood-pasture, and compared these to the genomes of the type strain and 21 other clinical strains. C. albicans strains from oak are similar to clinical C. albicans in that they are predominantly diploid and can become naturally homozygous at the mating locus through whole-chromosome loss of heterozygosity (LOH). LOH regions in all genomes arose recently suggesting that LOH mutations usually occur transiently in C. albicans populations. Oak strains differed from clinical strains in showing less LOH, and higher levels of heterozygosity genome-wide. Using phylogenomic analyses, in silico chromosome painting, and comparisons with thousands more C. albicans strains at seven loci, we show that each oak strain is more closely related to strains from humans and other animals than to strains from other oaks. Therefore, the isolation of C. albicans from oak is not easily explained as contamination from a single animal source. The high heterozygosity of oak strains could arise as a result of reduced mitotic recombination in asexual lineages, recent parasexual reproduction or because of natural selection. Regardless of mechanism, the diversity of C. albicans on oaks implies that they have lived in this environment long enough for genetic differences from clinical strains to arise.

genomics↗

Habitat predicts levels of genetic admixture in Saccharomyces cerevisiae

Genetic admixture can provide material for populations to adapt to local environments, and this process has played a crucial role in the domestication of plants and animals. The model yeast, Saccharomyces cerevisiae, has been domesticated multiple times for the production of wine, sake, beer and bread, but the high rate of admixture between yeast lineages has so far been treated as a complication for population genomic analysis. Here we make use of the low recombination rate at centromeres to investigate admixture in yeast using a classic Bayesian approach and a more conservative locus by locus phylogenetic approach developed here. Using both approaches, we find that S. cerevisiae from stable oak woodland habitats are less likely to show recent genetic admixture compared with those isolated from transient habitats such as fruits, wine or human infections. When woodland yeast strains do show recent genetic admixture, the degree of admixture is lower than in strains from other habitats. Furthermore, S. cerevisiae populations from oak woodlands are genetically isolated from each other, with only occasional migration between woodlands and local fruit habitats. Application of our phylogenetic approach suggests that there is a previously undetected population in North Africa that is the closest outgroup to the European S. cerevisiae, including the domesticated Wine population. Thorough testing for admixture in S. cerevisiae therefore leads to a better understanding of the underlying population structure of the species and will be important for understanding the selective processes underlying domestication in this economically important species.

evolutionary biology↗