Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae

Raquel Barbosa, Pedro Almeida, Silvana V. B. Safar, Renata Oliveira Santos, Paula B. Morais, Lou Nielly-Thibault, Jean Baptiste Leducq, Christian R. Landry, Paula Maria Theriaga Mendes Bernardo Gonçalves, Carlos A. Rosa, Jose Paulo Sampaio

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Abstract

The natural biology of Saccharomyces cerevisiae, the best known unicellular model eukaryote, remains poorly documented and understood although recent progress has started to change this situation. Studies carried out recently in the Northern Hemisphere revealed the existence of wild populations associated with oak trees in North America, Asia, and in the Mediterranean region. However, in spite of these advances, the global distribution of natural populations of S. cerevisiae, especially in regions were oaks and other members of the Fagaceae are absent, is not well understood. Here we investigate the occurrence of S. cerevisiae in Brazil, atropical region where oaks and other Fagaceae are absent. We report a candidate natural habitat of S. cerevisiae in South America and, using whole-genome data, we uncover new lineages that appear to have as closest relatives the wild populations found in North America and Japan. A population structure analysis revealed the penetration of the wine genotype into the wild Brazilian population, a first observation of the impact of domesticated microbe lineages on the genetic structure of wild populations. Unexpectedly, the Brazilian population shows conspicuous evidence of hybridization with an American population of Saccharomyces paradoxus. Introgressions from S. paradoxus were significantly enriched in genes encoding secondary active transmembrane transporters. We hypothesize that hybridization in tropical wild lineages may have facilitated the habitat transition accompanying the colonization of the tropical ecosystem.
Original languageEnglish
Pages (from-to)317-329
Number of pages13
JournalGenome Biology And Evolution
Volume8
Issue number2
DOIs
Publication statusPublished - Feb 2016

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wild population
Saccharomyces cerevisiae
hybridization
Fagaceae
Population
Ecosystem
introgression
eukaryote
habitat
Quercus
genetic structure
population structure
North America
Northern Hemisphere
genotype
penetration
colonization
genome
Northern Asia
Mediterranean Region

Keywords

  • POPULATION-STRUCTURE
  • EVOLUTIONARY GENETICS
  • MAXIMUM-LIKELIHOOD
  • SEQUENCE DIVERSITY
  • YEAST
  • PARADOXUS
  • DOMESTICATION
  • GENOME
  • STRAINS
  • ENVIRONMENTS

Cite this

Barbosa, R., Almeida, P., Safar, S. V. B., Santos, R. O., Morais, P. B., Nielly-Thibault, L., ... Sampaio, J. P. (2016). Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae. Genome Biology And Evolution, 8(2), 317-329. https://doi.org/10.1093/gbe/evv263
Barbosa, Raquel ; Almeida, Pedro ; Safar, Silvana V. B. ; Santos, Renata Oliveira ; Morais, Paula B. ; Nielly-Thibault, Lou ; Leducq, Jean Baptiste ; Landry, Christian R. ; Gonçalves, Paula Maria Theriaga Mendes Bernardo ; Rosa, Carlos A. ; Sampaio, Jose Paulo. / Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae. In: Genome Biology And Evolution. 2016 ; Vol. 8, No. 2. pp. 317-329.
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abstract = "The natural biology of Saccharomyces cerevisiae, the best known unicellular model eukaryote, remains poorly documented and understood although recent progress has started to change this situation. Studies carried out recently in the Northern Hemisphere revealed the existence of wild populations associated with oak trees in North America, Asia, and in the Mediterranean region. However, in spite of these advances, the global distribution of natural populations of S. cerevisiae, especially in regions were oaks and other members of the Fagaceae are absent, is not well understood. Here we investigate the occurrence of S. cerevisiae in Brazil, atropical region where oaks and other Fagaceae are absent. We report a candidate natural habitat of S. cerevisiae in South America and, using whole-genome data, we uncover new lineages that appear to have as closest relatives the wild populations found in North America and Japan. A population structure analysis revealed the penetration of the wine genotype into the wild Brazilian population, a first observation of the impact of domesticated microbe lineages on the genetic structure of wild populations. Unexpectedly, the Brazilian population shows conspicuous evidence of hybridization with an American population of Saccharomyces paradoxus. Introgressions from S. paradoxus were significantly enriched in genes encoding secondary active transmembrane transporters. We hypothesize that hybridization in tropical wild lineages may have facilitated the habitat transition accompanying the colonization of the tropical ecosystem.",
keywords = "POPULATION-STRUCTURE, EVOLUTIONARY GENETICS, MAXIMUM-LIKELIHOOD, SEQUENCE DIVERSITY, YEAST, PARADOXUS, DOMESTICATION, GENOME, STRAINS, ENVIRONMENTS",
author = "Raquel Barbosa and Pedro Almeida and Safar, {Silvana V. B.} and Santos, {Renata Oliveira} and Morais, {Paula B.} and Lou Nielly-Thibault and Leducq, {Jean Baptiste} and Landry, {Christian R.} and Gon{\cc}alves, {Paula Maria Theriaga Mendes Bernardo} and Rosa, {Carlos A.} and Sampaio, {Jose Paulo}",
note = "This work was supported by Fundacao para a Ciencia e a Tecnologia, Portugal, grants PTDC/BIA-EVF/118618/2010 (J.P.S., P.A., P.G.), PTDC/AGR-ALI/118590/2010 (J.P.S., P.A., P.G., R.B.), UID/Multi/04378/2013 (J.P.S., P.G.), and SFRH/BD/77390/2011 (P.A.), by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico-CNPq (CAR, process numbers 560715/2010-2 and 457499/2014-1, PBM process number 457443/2012-0) and Fundacao de Amparo a Pesquisa de Minas Gerais FAPEMIG and VALE S.A (CAR, process number RCP-00094-10). Work of C.R.L. on this project was supported by a NSERC Discovery grant. C.R.L. holds the Canada Research Chair in Evolutionary Cell and Systems Biology. The authors thank Dr. Siu Mui Tsai, Universidade de Sao Paulo, Brazil, for making available strain UFMG-CM-Y640.",
year = "2016",
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language = "English",
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Barbosa, R, Almeida, P, Safar, SVB, Santos, RO, Morais, PB, Nielly-Thibault, L, Leducq, JB, Landry, CR, Gonçalves, PMTMB, Rosa, CA & Sampaio, JP 2016, 'Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae', Genome Biology And Evolution, vol. 8, no. 2, pp. 317-329. https://doi.org/10.1093/gbe/evv263

Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae. / Barbosa, Raquel; Almeida, Pedro; Safar, Silvana V. B.; Santos, Renata Oliveira; Morais, Paula B.; Nielly-Thibault, Lou; Leducq, Jean Baptiste; Landry, Christian R.; Gonçalves, Paula Maria Theriaga Mendes Bernardo; Rosa, Carlos A.; Sampaio, Jose Paulo.

In: Genome Biology And Evolution, Vol. 8, No. 2, 02.2016, p. 317-329.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae

AU - Barbosa, Raquel

AU - Almeida, Pedro

AU - Safar, Silvana V. B.

AU - Santos, Renata Oliveira

AU - Morais, Paula B.

AU - Nielly-Thibault, Lou

AU - Leducq, Jean Baptiste

AU - Landry, Christian R.

AU - Gonçalves, Paula Maria Theriaga Mendes Bernardo

AU - Rosa, Carlos A.

AU - Sampaio, Jose Paulo

N1 - This work was supported by Fundacao para a Ciencia e a Tecnologia, Portugal, grants PTDC/BIA-EVF/118618/2010 (J.P.S., P.A., P.G.), PTDC/AGR-ALI/118590/2010 (J.P.S., P.A., P.G., R.B.), UID/Multi/04378/2013 (J.P.S., P.G.), and SFRH/BD/77390/2011 (P.A.), by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico-CNPq (CAR, process numbers 560715/2010-2 and 457499/2014-1, PBM process number 457443/2012-0) and Fundacao de Amparo a Pesquisa de Minas Gerais FAPEMIG and VALE S.A (CAR, process number RCP-00094-10). Work of C.R.L. on this project was supported by a NSERC Discovery grant. C.R.L. holds the Canada Research Chair in Evolutionary Cell and Systems Biology. The authors thank Dr. Siu Mui Tsai, Universidade de Sao Paulo, Brazil, for making available strain UFMG-CM-Y640.

PY - 2016/2

Y1 - 2016/2

N2 - The natural biology of Saccharomyces cerevisiae, the best known unicellular model eukaryote, remains poorly documented and understood although recent progress has started to change this situation. Studies carried out recently in the Northern Hemisphere revealed the existence of wild populations associated with oak trees in North America, Asia, and in the Mediterranean region. However, in spite of these advances, the global distribution of natural populations of S. cerevisiae, especially in regions were oaks and other members of the Fagaceae are absent, is not well understood. Here we investigate the occurrence of S. cerevisiae in Brazil, atropical region where oaks and other Fagaceae are absent. We report a candidate natural habitat of S. cerevisiae in South America and, using whole-genome data, we uncover new lineages that appear to have as closest relatives the wild populations found in North America and Japan. A population structure analysis revealed the penetration of the wine genotype into the wild Brazilian population, a first observation of the impact of domesticated microbe lineages on the genetic structure of wild populations. Unexpectedly, the Brazilian population shows conspicuous evidence of hybridization with an American population of Saccharomyces paradoxus. Introgressions from S. paradoxus were significantly enriched in genes encoding secondary active transmembrane transporters. We hypothesize that hybridization in tropical wild lineages may have facilitated the habitat transition accompanying the colonization of the tropical ecosystem.

AB - The natural biology of Saccharomyces cerevisiae, the best known unicellular model eukaryote, remains poorly documented and understood although recent progress has started to change this situation. Studies carried out recently in the Northern Hemisphere revealed the existence of wild populations associated with oak trees in North America, Asia, and in the Mediterranean region. However, in spite of these advances, the global distribution of natural populations of S. cerevisiae, especially in regions were oaks and other members of the Fagaceae are absent, is not well understood. Here we investigate the occurrence of S. cerevisiae in Brazil, atropical region where oaks and other Fagaceae are absent. We report a candidate natural habitat of S. cerevisiae in South America and, using whole-genome data, we uncover new lineages that appear to have as closest relatives the wild populations found in North America and Japan. A population structure analysis revealed the penetration of the wine genotype into the wild Brazilian population, a first observation of the impact of domesticated microbe lineages on the genetic structure of wild populations. Unexpectedly, the Brazilian population shows conspicuous evidence of hybridization with an American population of Saccharomyces paradoxus. Introgressions from S. paradoxus were significantly enriched in genes encoding secondary active transmembrane transporters. We hypothesize that hybridization in tropical wild lineages may have facilitated the habitat transition accompanying the colonization of the tropical ecosystem.

KW - POPULATION-STRUCTURE

KW - EVOLUTIONARY GENETICS

KW - MAXIMUM-LIKELIHOOD

KW - SEQUENCE DIVERSITY

KW - YEAST

KW - PARADOXUS

KW - DOMESTICATION

KW - GENOME

KW - STRAINS

KW - ENVIRONMENTS

U2 - 10.1093/gbe/evv263

DO - 10.1093/gbe/evv263

M3 - Article

VL - 8

SP - 317

EP - 329

JO - Genome Biology And Evolution

JF - Genome Biology And Evolution

SN - 1759-6653

IS - 2

ER -

Barbosa R, Almeida P, Safar SVB, Santos RO, Morais PB, Nielly-Thibault L et al. Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae. Genome Biology And Evolution. 2016 Feb;8(2):317-329. https://doi.org/10.1093/gbe/evv263