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Publications

Journal Article Ahead of print

PubMed: 42489507 DOI: 10.1093/molbev/msag187

Genetic background shapes the transcriptional activity and phenotypic contribution of a horizontally acquired region in yeast.

Mol Biol Evol

Authors: Andrés Romero, Camila Bastías, Matteo De Chiara, Xanita Saayman, Hajar Cherkaoui, Benjamin Barré, Francisco A Cubillos, Claudio Martínez, Eduardo I Kessi-Pérez, Gianni Liti, Francisco Salinas

Affiliations

  • Laboratorio de Genómica Funcional, Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile. ANID-Millennium Science Initiative-Millennium Institute for Integrative Biology (iBio), Santiago, Chile. Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France.
  • Centro de Estudios en Ciencia y Tecnología de Alimentos (CECTA), Universidad de Santiago de Chile (USACH), Santiago, Chile. Departamento de Ciencia y Tecnología de los Alimentos, Facultad Tecnológica, Universidad de Santiago de Chile (USACH), Santiago, Chile.
  • Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France.
  • ANID-Millennium Science Initiative-Millennium Institute for Integrative Biology (iBio), Santiago, Chile.
  • Departamento de Biología, Facultad de Química y Biología, Universidad de Santiago de Chile (USACH), Santiago, Chile.
  • ANID-Millennium Nucleus of Patagonian Limit of Life (LiLi), Valdivia, Chile.
  • Centro de Estudios en Ciencia y Tecnología de Alimentos (CECTA), Universidad de Santiago de Chile (USACH), Santiago, Chile.
  • Departamento de Ciencia y Tecnología de los Alimentos, Facultad Tecnológica, Universidad de Santiago de Chile (USACH), Santiago, Chile.
  • Laboratorio de Genómica Funcional, Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.

Abstract

Horizontal Gene Transfer (HGT) is the movement of genetic material across species. In Saccharomyces cerevisiae, a DNA segment known as Region B was acquired horizontally from a distant yeast species. This region (∼17 Kb) encodes 5 genes and is present in the genomes of yeast strains from different phylogenetic clades. Interestingly, the presence of Region B is not restricted to yeast strains isolated from fermentative environments, leaving its contribution to yeast niche-specific adaptation remains unclear. In this work, the genomic structure of Region B was analyzed in yeast strains from the ScRAP (Saccharomyces cerevisiae Reference Assembly Panel) collection, identifying 10 structural variants that maintain a circular continuity. To assess the role of Region B in yeast adaptation, we performed a high-throughput phenotyping of the ScRAP collection under different growth conditions, identifying that Region B is associated with higher tolerance to oxidative stress. Then, we characterized the transcriptional activity of each gene within Region B using a fluorescent reporter. The results revealed that gene expression depends on the host's genetic background and transcription factors encoded within Region B. To identify the genetic determinants involved in Region B expression within different genetic backgrounds, three expression Quantitative Trait Loci (eQTLs) were mapped and validated. Finally, by performing the deletion of Region B in two different strains, we determined a background-dependent contribution of this region to various fermentative phenotypes. Altogether, our results suggest a complex regulatory interaction between the horizontally acquired genes and the host genome that contributes to yeast adaptation under fermentation conditions.

MeSH

Genes, Yeasts, Molecular Biology, Genome, Genetic Background