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Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle.

ABSTRACT: Most microbes have complex life cycles with multiple modes of reproduction that differ in their effects on DNA sequence variation. Population genomic analyses can therefore be used to estimate the relative frequencies of these different modes in nature. The life cycle of the wild yeast Saccharomyces paradoxus is complex, including clonal reproduction, outcrossing, and two different modes of inbreeding. To quantify these different aspects we analyzed DNA sequence variation in the third chromosome among 20 isolates from two populations. Measures of mutational and recombinational diversity were used to make two independent estimates of the population size. In an obligately sexual population these values should be approximately equal. Instead there is a discrepancy of about three orders of magnitude between our two estimates of population size, indicating that S. paradoxus goes through a sexual cycle approximately once in every 1,000 asexual generations. Chromosome III also contains the mating type locus (MAT), which is the most outbred part in the entire genome, and by comparing recombinational diversity as a function of distance from MAT we estimate the frequency of matings to be approximately 94% from within the same tetrad, 5% with a clonemate after switching the mating type, and 1% outcrossed. Our study illustrates the utility of population genomic data in quantifying life cycles.

SUBMITTER: Tsai IJ

PROVIDER: S-EPMC2290798 | biostudies-literature | 2008 Mar

REPOSITORIES: biostudies-literature

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Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle.

Tsai Isheng J IJ Bensasson Douda D Burt Austin A Koufopanou Vassiliki V

Proceedings of the National Academy of Sciences of the United States of America 20080314 12

Most microbes have complex life cycles with multiple modes of reproduction that differ in their effects on DNA sequence variation. Population genomic analyses can therefore be used to estimate the relative frequencies of these different modes in nature. The life cycle of the wild yeast Saccharomyces paradoxus is complex, including clonal reproduction, outcrossing, and two different modes of inbreeding. To quantify these different aspects we analyzed DNA sequence variation in the third chromosome ...[more]

PMID: 18344325

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Project description:One might expect yeasts in soil to be highly dispersed via water or insects, forming ephemeral, genetically heterogeneous populations subject to competition and environmental stochasticity. Here, we report persistence of genotypes of the yeast Saccharomyces paradoxus in space and time. Within 1 km2 in a mixed hardwood forest on scales from centimeters to tens of meters, we detected persistence over 3 years of native genotypes, identified by single nucleotide polymorphisms (SNPs) genome-wide, of the wild yeast Saccharomyces paradoxus growing around Quercus rubra and Quercus alba Yeasts were recovered by enrichment in ethanol-containing medium, which measures only presence or absence, not abundance. Additional transplantation experiments employed strains marked with spontaneous defects in the URA3 gene, which also confer resistance to 5-fluoroorotic acid (5FOA). Plating soil suspensions from transplant sites on 5FOA-containing medium permitted one-step quantification of yeast CFU, with no interference from other unmarked yeasts or microorganisms. After an initial steep decrease in abundance, the yeast densities fluctuated over time, increasing in association with rainfall and decreasing in association with drought. After 18 months, the transplanted yeasts remained in place on the nine sites. In vitro transplantation experiments into nonsterile soil in petri dishes showed similar patterns of persistence and response to moisture and drought. To determine whether Saccharomyces cerevisiae, not previously recovered from soils regionally, can persist in our cold climate sites, we transplanted marked S. cerevisiae alone and in mixture with S. paradoxus in the fall of 2017. Five months later, S. cerevisiae persisted to the same extent as S. paradoxusIMPORTANCESaccharomyces yeasts are intensively studied in biological research and in their domesticated roles in brewing and baking, and yet, remarkably little is known about their mode of life in forest soils. We report here that resident genotypes of the yeast S. paradoxus are persistent on a time scale of years in their microhabitats in forest soils. We also show that resident genotypes can be replaced by transplanted yeast genotypes. The high inoculum levels in experimental transplantations rapidly decreased over time, but the transplanted genotypes persisted at low abundance. We conclude that, in forest soils, Saccharomyces yeasts exist at very low abundance and that dispersal events are rare.

Project description:Background: Recent studies have demonstrated that antisense transcription is pervasive in budding yeasts and is conserved between Saccharomyces cerevisiae and S. paradoxus. While studies have examined antisense transcripts of S. cerevisiae for inverse transcription in stationary phase and stress conditions, there is a lack of comprehensive analysis of the conditional specific evolutionary characteristics of antisense transcription between yeasts. Here we attempt to decipher the evolutionary relationship of antisense transcription of S. cerevisiae and S. paradoxus cultured in mid log, early stationary phase, and heat shock conditions. Results: Massively parallel sequencing of sequence strand-specific cDNA library was performed from RNA isolated from S. cerevisiae and S. paradoxus cells at mid log, stationary phase and heat shock conditions. We performed this analysis using a stringent set of sense ORF transcripts and non-coding antisense transcripts that were expressed in all the three conditions, as well as in both species. We found the divergence of the condition specific anti-sense transcription levels is higher than that in condition specific sense transcription levels, suggesting that antisense transcription played a potential role in adapting to different conditions. Furthermore, 43% of sense-antisense pairs demonstrated inverse transcription in either stationary phase or heat shock conditions relative to the mid log conditions. In addition, a large part of sense-antisense pairs (67%), which demonstrated inverse transcription, were highly conserved between the two species. Our results were also concordant with known functional analyses from previous studies and with the evidence from mechanistic experiments of role of individual genes. Conclusions: This study provides a comprehensive picture of the role of antisense transcription mediating sense transcription in different conditions across yeast species. We can conclude from our findings that antisense regulation could act like an on-off switch on sense regulation in different conditions.

Dataset Information

Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle.

Publications

Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle.

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