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A collection of barcoded natural isolates of Saccharomyces paradoxus to study microbial evolutionary ecology.

ABSTRACT: While the use of barcoded collections of laboratory microorganisms and the development of barcode-based cell tracking are rapidly developing in genetics and genomics research, tools to track natural populations are still lacking. The yeast Saccharomyces paradoxus is an emergent microbial model in ecology and evolution. More than five allopatric and sympatric lineages have been identified and hundreds of strains have been isolated for this species, allowing to assess the impact of natural diversity on complex traits. We constructed a collection of 550 barcoded and traceable strains of S. paradoxus, including all three North American lineages SpB, SpC, and SpC*. These strains are diploid, many have their genome fully sequenced and are barcoded with a unique 20 bp sequence that allows their identification and quantification. This yeast collection is functional for competitive experiments in pools as the barcodes allow to measure each lineage's and individual strains' fitness in common conditions. We used this tool to demonstrate that in the tested conditions, there are extensive genotype-by-environment interactions for fitness among S. paradoxus strains, which reveals complex evolutionary potential in variable environments. This barcoded collection provides a valuable resource for ecological genomics studies that will allow gaining a better understanding of S. paradoxus evolution and fitness-related traits.

SUBMITTER: Bleuven C

PROVIDER: S-EPMC6612553 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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A collection of barcoded natural isolates of Saccharomyces paradoxus to study microbial evolutionary ecology.

Bleuven Clara C Dubé Alexandre K AK Nguyen Guillaume Q GQ Gagnon-Arsenault Isabelle I Martin Hélène H Landry Christian R CR

MicrobiologyOpen 20181219 7

While the use of barcoded collections of laboratory microorganisms and the development of barcode-based cell tracking are rapidly developing in genetics and genomics research, tools to track natural populations are still lacking. The yeast Saccharomyces paradoxus is an emergent microbial model in ecology and evolution. More than five allopatric and sympatric lineages have been identified and hundreds of strains have been isolated for this species, allowing to assess the impact of natural diversi ...[more]

PMID: 30569485

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Project description:Microbes commonly exist in diverse and complex communities where species interact, and their genomic repertoires evolve over time. Our understanding of species interaction and evolution has increased during the last decades, but most studies of evolutionary dynamics are based on single species in isolation or in experimental systems composed of few interacting species. Here, we use the microbial ecosystem found in groundwater-fed sand filter as a model to avoid this limitation. In these open systems, diverse microbial communities experience relatively stable conditions, and the coupling between chemical and biological processes is generally well defined. Metagenomic analysis of 12 sand filters communities revealed systematic co-occurrence of at least five comammox Nitrospira species, likely promoted by low ammonium concentrations. These Nitrospira species showed intrapopulation sequence diversity, although possible clonal expansion was detected in a few abundant local comammox populations. Nitrospira species showed low homologous recombination and strong purifying selection, the latter process being especially strong in genes essential in energy metabolism. Positive selection was detected for genes related to resistance to foreign DNA and phages. We found that, compared to other habitats, groundwater-fed sand filters impose strong purifying selection and low recombination on comammox Nitrospira populations. These results suggest that evolutionary processes are more affected by habitat type than by species identity. Together, this study improves our understanding of species interaction and evolution in complex microbial communities and sheds light on the environmental dependency of evolutionary processes. IMPORTANCE Microbial species interact with each other and their environment (ecological processes) and undergo changes in their genomic repertoire over time (evolutionary processes). How these two classes of processes interact is largely unknown, especially for complex communities, as most studies of microbial evolutionary dynamics consider single species in isolation or a few interacting species in simplified experimental systems. In this study, these limitations are circumvented by examining the microbial communities found in stable and well-described groundwater-fed sand filters. Combining metagenomics and strain-level analyses, we identified the microbial interactions and evolutionary processes affecting comammox Nitrospira, a recently discovered bacterial type capable of performing the whole nitrification process. We found that abundant and co-occurrent Nitrospira populations in groundwater-fed sand filters are characterized by low recombination and strong purifying selection. In addition, by comparing these observations with those obtained from Nitrospira species inhabiting other environments, we revealed that evolutionary processes are more affected by habitat type than by species identity.

Project description:BackgroundTo characterize the genetic basis of phenotypic evolution, numerous studies have identified individual genes that have likely evolved under natural selection. However, phenotypic changes may represent the cumulative effect of similar evolutionary forces acting on functionally related groups of genes. Phylogenetic analyses of divergent yeast species have identified functional groups of genes that have evolved at significantly different rates, suggestive of differential selection on the functional properties. However, due to environmental heterogeneity over long evolutionary timescales, selection operating within a single lineage may be dramatically different, and it is not detectable via interspecific comparisons alone. Moreover, interspecific studies typically quantify selection on protein-coding regions using the D(n)/D(s) ratio, which cannot be extended easily to study selection on noncoding regions or synonymous sites. The population genetic-based analysis of selection operating within a single lineage ameliorates these limitations.FindingsWe investigated selection on several properties associated with genes, promoters, or polymorphic sites, by analyzing the derived allele frequency spectrum of single nucleotide polymorphisms (SNPs) in 28 strains of Saccharomyces paradoxus. We found evidence for significant differential selection between many functionally relevant categories of SNPs, underscoring the utility of function-centric approaches for discovering signatures of natural selection. When comparable, our findings are largely consistent with previous studies based on interspecific comparisons, with one notable exception: our study finds that mutations from an ancient amino acid to a relatively new amino acid are selectively disfavored, whereas interspecific comparisons have found selection against ancient amino acids. Several of our findings have not been addressed through prior interspecific studies: we find that synonymous mutations from preferred to unpreferred codons are selected against and that synonymous SNPs in the linker regions of proteins are relatively less constrained than those within protein domains.ConclusionsWe present the first global survey of selection acting on various functional properties in S. paradoxus. We found that selection pressures previously detected over long evolutionary timescales have also shaped the evolution of S. paradoxus. Importantly, we also make novel discoveries untenable via conventional interspecific analyses.

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

A collection of barcoded natural isolates of Saccharomyces paradoxus to study microbial evolutionary ecology.

Publications

A collection of barcoded natural isolates of Saccharomyces paradoxus to study microbial evolutionary ecology.

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