Amplification of the CUP1 gene is associated with evolution of copper tolerance in Saccharomyces cerevisiae

Adamo, Giusy Manuela; Lotti, Marina; Tamás, Markus J.; Brocca, Stefania

doi:10.1099/mic.0.058024-0

Cited by 53 publications

(50 citation statements)

References 67 publications

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“…Genes encoding for PAU proteins (a member of the seripauperin multigene family), copper resistance and salt tolerance related genes were found to be present in fewer copies in S. jurei genome compared to S. cerevisiae . This variation in copy number of genes in a genome can have phenotypic and physiological effects on the species (Landry et al 2006; Adamo et al 2012; Gorter de Vries et al 2017). …”

Section: Resultsmentioning

confidence: 99%

Whole Genome Sequencing,de NovoAssembly and Phenotypic Profiling for the New Budding Yeast SpeciesSaccharomyces jurei

Naseeb

Alsammar²,

Burgis

et al. 2018

G3 Genes|Genomes|Genetics

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Saccharomyces sensu stricto complex consist of yeast species, which are not only important in the fermentation industry but are also model systems for genomic and ecological analysis. Here, we present the complete genome assemblies of Saccharomyces jurei, a newly discovered Saccharomyces sensu stricto species from high altitude oaks. Phylogenetic and phenotypic analysis revealed that S. jurei is more closely related to S. mikatae, than S. cerevisiae, and S. paradoxus. The karyotype of S. jurei presents two reciprocal chromosomal translocations between chromosome VI/VII and I/XIII when compared to the S. cerevisiae genome. Interestingly, while the rearrangement I/XIII is unique to S. jurei, the other is in common with S. mikatae strain IFO1815, suggesting shared evolutionary history of this species after the split between S. cerevisiae and S. mikatae. The number of Ty elements differed in the new species, with a higher number of Ty elements present in S. jurei than in S. cerevisiae. Phenotypically, the S. jurei strain NCYC 3962 has relatively higher fitness than the other strain NCYC 3947T under most of the environmental stress conditions tested and showed remarkably increased fitness in higher concentration of acetic acid compared to the other sensu stricto species. Both strains were found to be better adapted to lower temperatures compared to S. cerevisiae.

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Section: Resultsmentioning

confidence: 99%

Whole Genome Sequencing,de NovoAssembly and Phenotypic Profiling for the New Budding Yeast SpeciesSaccharomyces jurei

Naseeb

Alsammar²,

Burgis

et al. 2018

G3 Genes|Genomes|Genetics

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“…CUP1 exists as a tandem repeat in the S288C genome, and adaptation under copper stress has previously been shown to select for amplification of this locus (Fogel and Welch 1982;Adamo et al 2012). Indeed, Covo et al (2014) recently demonstrated that moving CUP1 onto other chromosomes can efficiently select for disomy under copper stress.…”

Section: Discussionmentioning

confidence: 99%

“…CUP1 is a metallothionein protein that binds copper in S. cerevisiae. It is present as a tandem duplication on chrVIII in the S288C reference strain, and amplification of this locus is known to be a common mutation that confers increased resistance to copper (Fogel and Welch 1982;Fogel et al 1983;Adamo et al 2012). Disomy for chrVIII has also been shown to increase copper tolerance (Fogel and Welch 1982).…”

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confidence: 99%

Too Much of a Good Thing: The Unique and Repeated Paths Toward Copper Adaptation

Gerstein

Ono

et al. 2014

Genetics

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Copper is a micronutrient essential for growth due to its role as a cofactor in enzymes involved in respiration, defense against oxidative damage, and iron uptake. Yet too much of a good thing can be lethal, and yeast cells typically do not have tolerance to copper levels much beyond the concentration in their ancestral environment. Here, we report a short-term evolutionary study of Saccharomyces cerevisiae exposed to levels of copper sulfate that are inhibitory to the initial strain. We isolated and identified adaptive mutations soon after they arose, reducing the number of neutral mutations, to determine the first genetic steps that yeast take when adapting to copper. We analyzed 34 such strains through whole-genome sequencing and by assaying fitness within different environments; we also isolated a subset of mutations through tetrad analysis of four lines. We identified a multilayered evolutionary response. In total, 57 single base-pair mutations were identified across the 34 lines. In addition, gene amplification of the copper metallothionein protein, CUP1-1, was rampant, as was chromosomal aneuploidy. Four other genes received multiple, independent mutations in different lines (the vacuolar transporter genes VTC1 and VTC4; the plasma membrane H+-ATPase PMA1; and MAM3, a protein required for normal mitochondrial morphology). Analyses indicated that mutations in all four genes, as well as CUP1-1 copy number, contributed significantly to explaining variation in copper tolerance. Our study thus finds that evolution takes both common and less trodden pathways toward evolving tolerance to an essential, but highly toxic, micronutrient.KEYWORDS Saccharomyces cerevisiae; genetic basis of adaptation; copper tolerance; aneuploidy; CUP1; fitness; parallel adaptation I N his book, Wonderful Life (Gould 1989, p. 51), Stephen J. Gould famously opined that evolution is a historical and contingent process, so much so that "any replay of the tape would lead evolution down a pathway radically different from the road actually taken." While this is undoubtedly true when one considers the full complexity of an organism, refrains are often observed in evolution at the trait level. Repeated evolution, defined as "the independent appearance of similar phenotypic traits in distinct evolutionary lineages" (Gompel and Prud'homme 2009) has been documented in both ecological and clinical environments at all taxonomic levels, e.g., repeated loss of stickleback lateral plates in freshwater (Schluter et al. 2004), ecomorphs of Anolis lizards (Losos 1992), the acquisition of "cystic fibrosis lung" phenotypes in Pseudomonas aeruginosa in patients with cystic fibrosis (Huse et al. 2010), to name but a few. The development of sequencing technologies has recently allowed biologists to ask whether parallel genetic changes underlie observations of parallel phenotypic change. In some cases, parallel phenotypic evolution has been attributed to parallel genotypic evolution, for example, repeated changes to cis-regulatory regions of the same...

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“…The common laboratory strain S288c and many other Cu-tolerant strains contain independent amplifications of the CUP1 locus 27,39 . Other studies have also found that laboratory-evolved strains amplify this region of the genome 45 . The Saccharomyces Genome Database reference strain, S288c, has two alleles of CUP1 with YHR054c , a gene of unknown function, between them.…”

Section: Resultsmentioning

confidence: 88%

Proteomic and genetic analysis of the response of S. cerevisiae to soluble copper leads to improvement of the antimicrobial function of cellulosic copper nanoparticles

et al. 2017

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Copper (Cu) was used in antiquity to prevent waterborne and food diseases because, as a broad-spectrum antimicrobial agent, it generates reactive oxygen species, ROS. New technologies incorporating Cu into low-cost biodegradable nanomaterials built on cellulose, known as cellulosic cupric nanoparticles or c-CuNPs, present novel approaches to deliver Cu in a controlled manner to control microbial growth. We challenged strains of Saccharomyces cerevisiae to soluble Cu and c-CuNPs to evaluate the potential of c-CuNPs as antifungal agents. Cells exposed to c-CuNPs demonstrated greater sensitivity to Cu than cells exposed to soluble Cu, although Cu-resistant strains were more tolerant than Cu-sensitive strains of c-CuNP exposure. At the same level of growth inhibition, 157 μM c-CuNP led to the same internal Cu levels as did 400 CuSO4, offering evidence for alternative mechanisms of toxicity, perhaps through β-arrestin dependent endocytosis, which was supported by flow cytometry and fluorescence microscopy of c-CuNPs distributed both on the cell surface and within the cytoplasm. Genes responsible for genetic variation to copper were mapped to the ZRT2 and the CUP1 loci. Through proteomic analyses, we found that the expression of other zinc (Zn) transporters increased in Cu-tolerant yeast compared to Cu-sensitive strains. Further, the addition of Zn at low levels increased the potency of c-CuNP to inhibit even the most Cu-tolerant yeast. Through unbiased systems biological approaches, we identified Zn as a critical component of yeast response to Cu and the addition of Zn increased potency of the c-CuNPs.

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Amplification of the CUP1 gene is associated with evolution of copper tolerance in Saccharomyces cerevisiae

Cited by 53 publications

References 67 publications

Whole Genome Sequencing,de NovoAssembly and Phenotypic Profiling for the New Budding Yeast SpeciesSaccharomyces jurei

Whole Genome Sequencing,de NovoAssembly and Phenotypic Profiling for the New Budding Yeast SpeciesSaccharomyces jurei

Too Much of a Good Thing: The Unique and Repeated Paths Toward Copper Adaptation

Proteomic and genetic analysis of the response of S. cerevisiae to soluble copper leads to improvement of the antimicrobial function of cellulosic copper nanoparticles

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