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      Genomic Adaptation of Saccharomyces Species to Industrial Environments

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          Abstract

          The budding yeast has been extensively studied for its physiological performance in fermentative environments and, due to its remarkable plasticity, is used in numerous industrial applications like in brewing, baking and wine fermentations. Furthermore, thanks to its small and relatively simple eukaryotic genome, the molecular mechanisms behind its evolution and domestication are more easily explored. Considerable work has been directed into examining the industrial adaptation processes that shaped the genotypes of species and hybrids belonging to the Saccharomyces group, specifically in relation to beverage fermentation performances. A variety of genetic mechanisms are responsible for the yeast response to stress conditions, such as genome duplication, chromosomal re-arrangements, hybridization and horizontal gene transfer, and these genetic alterations are also contributing to the diversity in the Saccharomyces industrial strains. Here, we review the recent genetic and evolutionary studies exploring domestication and biodiversity of yeast strains.

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          Population genomics of domestic and wild yeasts

          Since the completion of the genome sequence of Saccharomyces cerevisiae in 19961,2, there has been an exponential increase in complete genome sequences accompanied by great advances in our understanding of genome evolution. Although little is known about the natural and life histories of yeasts in the wild, there are an increasing number of studies looking at ecological and geographic distributions3,4, population structure5-8, and sexual versus asexual reproduction9,10. Less well understood at the whole genome level are the evolutionary processes acting within populations and species leading to adaptation to different environments, phenotypic differences and reproductive isolation. Here we present one- to four-fold or more coverage of the genome sequences of over seventy isolates of the baker's yeast, S. cerevisiae, and its closest relative, S. paradoxus. We examine variation in gene content, SNPs, indels, copy numbers and transposable elements. We find that phenotypic variation broadly correlates with global genome-wide phylogenetic relationships. Interestingly, S. paradoxus populations are well delineated along geographic boundaries while the variation among worldwide S. cerevisiae isolates shows less differentiation and is comparable to a single S. paradoxus population. Rather than one or two domestication events leading to the extant baker's yeasts, the population structure of S. cerevisiae consists of a few well-defined geographically isolated lineages and many different mosaics of these lineages, supporting the idea that human influence provided the opportunity for cross-breeding and production of new combinations of pre-existing variation.
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            Horizontal gene transfer in eukaryotic evolution.

            Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.
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              Genome evolution across 1,011 Saccharomyces cerevisiae isolates

              Large-scale population genomic surveys are essential to explore the phenotypic diversity of natural populations. Here we report the whole-genome sequencing and phenotyping of 1,011 Saccharomyces cerevisiae isolates, which together provide an accurate evolutionary picture of the genomic variants that shape the species-wide phenotypic landscape of this yeast. Genomic analyses support a single ‘out-of-China’ origin for this species, followed by several independent domestication events. Although domesticated isolates exhibit high variation in ploidy, aneuploidy and genome content, genome evolution in wild isolates is mainly driven by the accumulation of single nucleotide polymorphisms. A common feature is the extensive loss of heterozygosity, which represents an essential source of inter-individual variation in this mainly asexual species. Most of the single nucleotide polymorphisms, including experimentally identified functional polymorphisms, are present at very low frequencies. The largest numbers of variants identified by genome-wide association are copy-number changes, which have a greater phenotypic effect than do single nucleotide polymorphisms. This resource will guide future population genomics and genotype–phenotype studies in this classic model system.
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                Author and article information

                Contributors
                Journal
                Front Genet
                Front Genet
                Front. Genet.
                Frontiers in Genetics
                Frontiers Media S.A.
                1664-8021
                27 August 2020
                2020
                : 11
                : 916
                Affiliations
                [1] 1Manchester Institute of Biotechnology, Faculty of Biology, Medicine and Health, The University of Manchester , Manchester, United Kingdom
                [2] 2Cloudwater Brew Co. , Manchester, United Kingdom
                Author notes

                Edited by: Francisco A. Cubillos, University of Santiago, Chile

                Reviewed by: Alexander DeLuna, Instituto Politécnico Nacional de México (CINVESTAV), Mexico; Marti Aldea, Instituto de Biología Molecular de Barcelona (IBMB), Spain

                *Correspondence: Daniela Delneri, d.delneri@ 123456manchester.ac.uk

                This article was submitted to Evolutionary and Genomic Microbiology, a section of the journal Frontiers in Genetics

                Article
                10.3389/fgene.2020.00916
                7481385
                33193572
                12f58bf8-91f7-4340-862e-7cb9d88cf52c
                Copyright © 2020 Giannakou, Cotterrell and Delneri.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 April 2020
                : 23 July 2020
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 109, Pages: 10, Words: 0
                Funding
                Funded by: H2020 Marie Skłodowska-Curie Actions 10.13039/100010665
                Funded by: Innovate UK 10.13039/501100006041
                Categories
                Genetics
                Mini Review

                Genetics
                fermentation,saccharomyces,adaptation,diversity,evolution
                Genetics
                fermentation, saccharomyces, adaptation, diversity, evolution

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