Mitochondrial DNA and temperature tolerance in lager yeasts

Baker, E.N.; Peris, David; Moriarty, Ryan V.; Li, Xueying C.; Fay, Justin C.; Hittinger, Chris Todd

doi:10.1101/391946

Cited by 17 publications

(22 citation statements)

References 52 publications

(33 reference statements)

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“…The natural hybrid S. pastorianus (hybridized from S. cerevisiae and S. eubayanus ) carries the S. eubayanus mitochondria (E. Baker et al 2015; Okuno et al 2016), while other industrial hybrids of Saccharomyces species used in wine and cider production have retained S. cerevisiae mitochondrial genome (Masneuf et al 1998). It has also recently been shown that the type of mitochondria inherited affects the phenotype (Albertin et al 2013; E. P. Baker et al 2019; X. C. Li et al 2019) and the transcriptional network (Hewitt et al 2020) in hybrids. Therefore, here, each of the tetraploid hybrids constructed were also selected for different mitotypes.…”

Section: Resultsmentioning

confidence: 99%

Restoring fertility in yeast hybrids: breeding and quantitative genetics of beneficial traits

Naseeb

Visinoni

et al. 2021

Preprint

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Hybrids species can harbour a combination of beneficial traits from each parent and may exhibit hybrid vigour, more readily adapting to new harsher environments. Inter-species hybrids are also sterile and therefore an evolutionary dead-end unless fertility is restored, usually via auto-polyploidisation events. In the Saccharomyces genus, hybrids are readily found in nature and in industrial settings, where they have adapted to severe fermentative conditions. Due to their hybrid sterility, the development of new commercial yeast strains has so far been primarily conducted via selection methods rather than breeding. In this study, we overcame infertility by creating tetraploid intermediates of Saccharomyces inter-species hybrids, to allow continuous multigenerational breeding. We incorporated nuclear and mitochondrial genetic diversity within each parental species, allowing for quantitative genetic analysis of traits exhibited by the hybrids, and for nuclear-mitochondrial interactions to be assessed. Using pooled F12 generation segregants of different hybrids with extreme phenotype distributions, we identified QTLs for tolerance to high and low temperatures, high sugar concentration, high ethanol concentration, and acetic acid levels. We identified QTLs that are species specific, that are shared between species, as well as hybrid specific, where the variants do not exhibit phenotypic differences in the original parental species. Moreover, we could distinguish between mitochondria-type dependent and independent traits. This study tackles the complexity of the genetic interactions and traits in hybrid species, bringing hybrids into the realm of full genetic analysis of diploid species, and paves the road for the biotechnological exploitation of yeast biodiversity.

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Section: Resultsmentioning

confidence: 99%

Restoring fertility in yeast hybrids: breeding and quantitative genetics of beneficial traits

Naseeb

Visinoni

et al. 2021

Preprint

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“…Our results suggest that mtDNA has played an important role in divergence of thermal growth profiles among the Saccharomyces species, with heat tolerance evolving primarily on the lineage leading to S. cerevisiae and cold tolerance evolving primarily on the lineage leading to S. uvarum. A related study has shown these differences have had a direct impact on the domestication of lagerbrewing yeast hybrids (Baker et al 2018)…”

Section: A Non-complementation Screen For Thermosensitive Alleles Revmentioning

confidence: 99%

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Peris

et al. 2018

Preprint

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Over time, species evolve substantial phenotype differences. Yet, genetic analysis of these traits is limited by reproductive barriers to those phenotypes that distinguish closely related species. Here, we conduct a genome-wide non-complementation screen to identify genes that contribute to a major difference in thermal growth profile between two Saccharomyces species. S. cerevisiae is capable of growing at temperatures exceeding 40C, whereas S. uvarum cannot grow above 33C but outperforms S. cerevisiae at 4C. The screen revealed only a single nuclear-encoded gene with a modest contribution to heat tolerance, but a large effect of the species' mitochondrial DNA (mitotype). Furthermore, we found that, while the S. cerevisiae mitotype confers heat tolerance, the S. uvarum mitotype confers cold tolerance. Recombinant mitotypes indicate multiple genes contribute to thermal divergence. Mitochondrial allele replacements showed that divergence in the coding sequence of COX1 has a moderate effect on both heat and cold tolerance, but it does not explain the entire difference between the two mitochondrial genomes. Our results highlight a polygenic architecture for interspecific phenotypic divergence and point to the mitochondrial genome as an evolutionary hotspot for not only reproductive incompatibilities, but also thermal divergence in yeast.

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“…With mitochondria, previous studies have indicated that the mitochondrial genome plays an important role in yeast thermal adaptation [47][48][49] . We found that out of the 9 unstable enzymes identified with the Posterior etcGEMs (with a Tm lower than 42 °C, Fig S7), three (ATP1, HEM1 and PDB1) belonged to the mitochondrial energy metabolism.…”

Section: Discussionmentioning

confidence: 99%

Bayesian genome scale modelling identifies thermal determinants of yeast metabolism

Wang

et al. 2020

Preprint

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The molecular basis of how temperature affects cell metabolism has been a long-standing question in biology, where the main obstacles are the lack of high-quality data and methods to associate temperature effects on the function of individual proteins as well as to combine them at a systems level. Here we develop and apply a Bayesian modeling approach to resolve the temperature effects in genome scale metabolic models (GEM). The approach minimizes uncertainties in enzymatic thermal parameters and greatly improves the predictive strength of the GEMs. The resulting temperature constrained yeast GEM uncovered enzymes that limit growth at superoptimal temperatures, and squalene epoxidase (ERG1) was predicted to be the most rate limiting. By replacing this single key enzyme with an ortholog from a thermotolerant yeast strain, we obtained a thermotolerant strain that outgrew the wild type, demonstrating the critical role of sterol metabolism in yeast thermosensitivity. Therefore, apart from identifying thermal determinants of cell metabolism and enabling the design of thermotolerant strains, our Bayesian GEM approach facilitates modelling of complex biological systems in the absence of high-quality data and therefore shows promise for becoming a standard tool for genome scale modeling.Temperature is the most common environmental and evolutionary factor that shapes the physiology of living cells. Organisms have successfully adapted to survive in diverse temperature ranges 1-3 , where minor deviations from the optimal temperature by merely a few degrees can dramatically impair cell growth. For instance, the model eukaryotic organism Saccharomyces cerevisiae has an optimal growth temperature of ~30°C, whereas a temperature of 42°C is already lethal to the organism 4,5 . Since cell growth fundamentally requires all cellular components to be functional in the temperature window of cell growth, proteins, the most abundant group of biomolecules that carry out the majority of catalytic functions and are also the most sensitive to changes in temperature 5-7 , are considered to have the largest effect on cell physiology in relation to temperature. However, despite all our knowledge of temperature effects at both the cellular and molecular levels, including recent breakthroughs in temperature-dependent protein folding 7-10 and enzyme kinetics 11,12 , the temperature association between proteins and cell physiology is still poorly understood.Multiple studies have attempted to model the temperature effects on cell growth with very few proteome wide parameters. For instance, the dominant activation barrier and the number of essential proteins to cell growth 13 , activation energy of the growth process and the free energy change of protein denaturation 14 and others (reviewed in 15 ). These models showed excellent performance when describing the general cell growth rate at various temperatures, however, they could not pinpoint the specific rate-limiting enzymes, nor predict the amount of improvement in growth rate by replacing these ...

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Mitochondrial DNA and temperature tolerance in lager yeasts

Cited by 17 publications

References 52 publications

Restoring fertility in yeast hybrids: breeding and quantitative genetics of beneficial traits

Restoring fertility in yeast hybrids: breeding and quantitative genetics of beneficial traits

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Bayesian genome scale modelling identifies thermal determinants of yeast metabolism

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