SO 2 and copper tolerance exhibit an evolutionary trade-off in Saccharomyces cerevisiae

PLOS Genetics · 12 authors, 3 centres

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TL;DR

The study used genetic and biochemical methods to investigate why high copper tolerance and high SO2 tolerance are mutually exclusive in wine yeast. It found that over-expression of the SO2 tolerance gene SSU1 causes sulfur limitation, making yeast highly sensitive to copper, especially in low-sulfur environments.

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This preclinical study used Saccharomyces cerevisiae wine yeast strains to investigate the negative genetic association between copper tolerance (linked to CUP1 copy number) and SO2 tolerance (linked to SSU1 over-expression). Methods included bulk-segregant QTL analysis, reciprocal hemizygosity analysis, transcriptional and proteomic analysis, and growth/fermentation assays under controlled copper and sulfate concentrations. The central result is that SSU1 over-expression induces sulfur limitation, which burdens the sulfate assimilation pathway. This was experimentally demonstrated by showing that an SSU1 over-expressing strain (AWRI 4052) exhibited severely impaired growth and fermentation in the presence of moderately elevated copper when sulfate was limited (20 mg/L), while a control strain was unaffected. The study concludes that copper and SO2 tolerance are conditional traits, providing evidence for a metabolic basis for their mutual exclusivity and suggesting an evolutionary driver for extreme CUP1 amplification.

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other

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preclinical research

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ORIGINAL PAPER

PMC10081759

SO 2 and copper tolerance exhibit an evolutionary trade-off in Saccharomyces cerevisiae

PLOS Genetics

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ABSTRACT

Abstract Copper tolerance and SO 2 tolerance are two well-studied phenotypic traits of Saccharomyces cerevisiae . The genetic bases of these traits are the allelic expansion at the CUP1 locus and reciprocal translocation at the SSU1 locus, respectively. Previous work identified a negative association between SO 2 and copper tolerance in S . cerevisiae wine yeasts. Here we probe the relationship between SO 2 and copper tolerance and show that an increase in CUP1 copy number does not always impart copper tolerance in S . cerevisiae wine yeast. Bulk-segregant QTL analysis was used to identify variance at SSU1 as a causative factor in copper sensitivity, which was verified by reciprocal hemizygosity analysis in a strain carrying 20 copies of CUP1 . Transcriptional and proteomic analysis demonstrated that SSU1 over-expression did not suppress CUP1 transcription or constrain protein production and provided evidence that SSU1 over-expression induced sulfur limitation during exposure to copper. Finally, an SSU1 over-expressing strain exhibited increased sensitivity to moderately elevated copper concentrations in sulfur-limited medium, demonstrating that SSU1 over-expression burdens the sulfate assimilation pathway. Over-expression of MET 3/14/16 , genes upstream of H 2 S production in the sulfate assimilation pathway increased the production of SO 2 and H 2 S but did not improve copper sensitivity in an SSU1 over-expressing background. We conclude that copper and SO 2 tolerance are conditional traits in S . cerevisiae and provide evidence of the metabolic basis for their mutual exclusivity. These findings suggest an evolutionary driver for the extreme amplification of CUP1 observed in some yeasts.

CITATION EXPORT

Cristobal A Onetto, Dariusz R Kutyna, Radka Kolouchova et al.. SO2 and copper tolerance exhibit an evolutionary trade-off in Saccharomyces cerevisiae. PLOS Genetics. (2023). https://doi.org/10.1371/journal.pgen.1010692

AUTHORS

12 · 3 CENTRES

Cristobal A Onetto, Dariusz R Kutyna, Radka Kolouchova, Jane McCarthy, Anthony R Borneman, Simon A Schmidt, Justin C Fay, Geraldine Butler, Justin C Fay, Geraldine Butler, Justin C Fay, Geraldine Butler

1The Australian Wine Research Institute, Glen Osmond, South Australia, Australia
2School of Agriculture, Food and Wine, Faculty of Sciences, University of Adelaide, Adelaide, South Australia, Australia
3University of Rochester, UNITED STATES