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      Mitochondrial DNA and temperature tolerance in lager yeasts

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          Abstract

          Mitochondrial genome origin affects the temperature tolerance of synthetic and industrial lager-brewing yeast hybrids.

          Abstract

          A growing body of research suggests that the mitochondrial genome (mtDNA) is important for temperature adaptation. In the yeast genus Saccharomyces, species have diverged in temperature tolerance, driving their use in high- or low-temperature fermentations. Here, we experimentally test the role of mtDNA in temperature tolerance in synthetic and industrial hybrids ( Saccharomyces cerevisiae × Saccharomyces eubayanus or Saccharomyces pastorianus), which cold-brew lager beer. We find that the relative temperature tolerances of hybrids correspond to the parent donating mtDNA, allowing us to modulate lager strain temperature preferences. The strong influence of mitotype on the temperature tolerance of otherwise identical hybrid strains provides support for the mitochondrial climactic adaptation hypothesis in yeasts and demonstrates how mitotype has influenced the world’s most commonly fermented beverage.

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          Most cited references46

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Natural selection shaped regional mtDNA variation in humans.

            Human mtDNA shows striking regional variation, traditionally attributed to genetic drift. However, it is not easy to account for the fact that only two mtDNA lineages (M and N) left Africa to colonize Eurasia and that lineages A, C, D, and G show a 5-fold enrichment from central Asia to Siberia. As an alternative to drift, natural selection might have enriched for certain mtDNA lineages as people migrated north into colder climates. To test this hypothesis we analyzed 104 complete mtDNA sequences from all global regions and lineages. African mtDNA variation did not significantly deviate from the standard neutral model, but European, Asian, and Siberian plus Native American variations did. Analysis of amino acid substitution mutations (nonsynonymous, Ka) versus neutral mutations (synonymous, Ks) (kaks) for all 13 mtDNA protein-coding genes revealed that the ATP6 gene had the highest amino acid sequence variation of any human mtDNA gene, even though ATP6 is one of the more conserved mtDNA proteins. Comparison of the kaks ratios for each mtDNA gene from the tropical, temperate, and arctic zones revealed that ATP6 was highly variable in the mtDNAs from the arctic zone, cytochrome b was particularly variable in the temperate zone, and cytochrome oxidase I was notably more variable in the tropics. Moreover, multiple amino acid changes found in ATP6, cytochrome b, and cytochrome oxidase I appeared to be functionally significant. From these analyses we conclude that selection may have played a role in shaping human regional mtDNA variation and that one of the selective influences was climate.
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              Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast.

              Domestication of plants and animals promoted humanity's transition from nomadic to sedentary lifestyles, demographic expansion, and the emergence of civilizations. In contrast to the well-documented successes of crop and livestock breeding, processes of microbe domestication remain obscure, despite the importance of microbes to the production of food, beverages, and biofuels. Lager-beer, first brewed in the 15th century, employs an allotetraploid hybrid yeast, Saccharomyces pastorianus (syn. Saccharomyces carlsbergensis), a domesticated species created by the fusion of a Saccharomyces cerevisiae ale-yeast with an unknown cryotolerant Saccharomyces species. We report the isolation of that species and designate it Saccharomyces eubayanus sp. nov. because of its resemblance to Saccharomyces bayanus (a complex hybrid of S. eubayanus, Saccharomyces uvarum, and S. cerevisiae found only in the brewing environment). Individuals from populations of S. eubayanus and its sister species, S. uvarum, exist in apparent sympatry in Nothofagus (Southern beech) forests in Patagonia, but are isolated genetically through intrinsic postzygotic barriers, and ecologically through host-preference. The draft genome sequence of S. eubayanus is 99.5% identical to the non-S. cerevisiae portion of the S. pastorianus genome sequence and suggests specific changes in sugar and sulfite metabolism that were crucial for domestication in the lager-brewing environment. This study shows that combining microbial ecology with comparative genomics facilitates the discovery and preservation of wild genetic stocks of domesticated microbes to trace their history, identify genetic changes, and suggest paths to further industrial improvement.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                January 2019
                30 January 2019
                : 5
                : 1
                : eaav1869
                Affiliations
                [1 ]Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin–Madison, Madison, WI, USA.
                [2 ]Microbiology Doctoral Training Program, University of Wisconsin–Madison, Madison, WI, USA.
                [3 ]DOE Great Lakes Bioenergy Research Center, University of Wisconsin–Madison, Madison, WI, USA.
                [4 ]Department of Food Biotechnology, Institute of Agrochemistry and Food Technology (IATA), CSIC, Paterna, Valencia, Spain.
                [5 ]Molecular Genetics and Genomics Program, Washington University, St. Louis, MO, USA.
                [6 ]Department of Genetics, Washington University, St. Louis, MO, USA.
                [7 ]Center for Genome Sciences and System Biology, Washington University, St. Louis, MO, USA.
                [8 ]Department of Biology, University of Rochester, Rochester, NY, USA.
                Author notes
                [* ]Corresponding author. Email: cthittinger@ 123456wisc.edu
                Author information
                http://orcid.org/0000-0002-7875-2144
                http://orcid.org/0000-0001-9912-8802
                http://orcid.org/0000-0001-7100-1906
                http://orcid.org/0000-0002-1100-4694
                http://orcid.org/0000-0003-1893-877X
                http://orcid.org/0000-0001-5088-7461
                Article
                aav1869
                10.1126/sciadv.aav1869
                6353617
                30729163
                5d2582e1-2e6b-48d2-a0c1-fd063d39052b
                Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 22 August 2018
                : 03 January 2019
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB-1253634
                Funded by: doi http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: GM080669
                Funded by: doi http://dx.doi.org/10.13039/100000875, Pew Charitable Trusts;
                Award ID: Pew Scholar in the Biomedical Sciences
                Funded by: DOE Great Lakes Bioenergy Research Center;
                Award ID: DE-SC0018409
                Funded by: DOE Great Lakes Bioenergy Research Center;
                Award ID: DE-FC02-07ER64494
                Funded by: Vilas Trust Estate;
                Award ID: Vilas Faculty Early Career Investigator
                Funded by: United States Department of Agriculture National Institute of Food and Agriculture;
                Award ID: Hatch project 1003258
                Funded by: Marie Sklodowska-Curie Fellow;
                Award ID: 747775
                Funded by: Louis and Elsa Thomsen Wisconsin Distinguished Graduate Fellowship;
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