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The rise of the yeast genus Saccharomyces:
biodiversity and evolution
David Peris, Postdoctoral Marie Curie Fellow
Biotechnology Department, SBYBI Group (IATA-CSIC)
23th September 2019
@djperis
Saccharomyces cerevisiae as a species model
Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html
Well characterize eukaryotic cell
Saccharomyces cerevisiae as a species model
Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html
Small genome
Well characterize eukaryotic cell
Saccharomyces cerevisiae as a species model
Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html
Easy to manipulate
Small genome
Well characterize eukaryotic cell
Saccharomyces cerevisiae as a species model
Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html
Easy to manipulate
Small genome
Similarities to other
eukaryotes
Well characterize eukaryotic cell
S. cerevisiae is important for their multiple applications!
Ales
Traditional
beverages
Wine
Cider
Sake
In rich conditions, yeast divides by mitosis
Haploid (n) Haploid (n) Diploid (2n)
Clonal divisions (mitosis)
How do we define a species? Life cycle
MAT MATa MAT/MATa
Haploid (n) Haploid (n) Diploid (2n)
2 Sexual types (MAT locus)
Sexual competent cells can mate
MAT MATa MAT/MATa
Haploid (n) Haploid (n) Diploid (2n)
MAT MATa
X
MAT/MATa
schmoo
MATa
MAT
MATa MAT
Sporulation is promoted under starvation or stressful conditions
MAT/MATa
Diploid (2n)


a
a
Tetrad
Spore
Sporulation
A diploid gets sexual competent by sporulating
MAT/MATa
Diploid (2n)
MAT MATa
X
MAT/MATa


a
a
MAT
X
MAT/MATa
MATa


a
a
x x x x
x x x x
x x x x
x x x x
x x x x
x x x
x x x x
x x x x
x x x x
x x x x
x x x x
x x x x
x x x
x x x x
x x x x
x x x x
x x x x
x x x
x x x x
x x x x
x x x x
x x x x
x x x
x x x x
x x x x
x x x x
x x x x
x x x x
x x x x
x x x x
x x x x
x x x x
x: No growth
4/128 = 3.1%
If spore viability below 5% suggests different species (postzygotic barrier)
MAT/MATa


a
MAT/MATa
a


a
a
Saccharomyces genomes 1.0
S. paradoxus
S. mikatae
S. kudriavzevii
S. uvarum
S. cerevisiae
Scannell et al 2011
The genus Saccharomyces
Libkind et al 2011
Liti et al 2013
Naseeb et al 2018
S. paradoxus
S. mikatae
S. arboricola
S. kudriavzevii
S. uvarum
S. cerevisiae
S. eubayanus
S. jureii
Two stories
Population genomics of Saccharomyces eubayanus
The Saccharomyces genus as a model
S. cerevisiae
S. paradoxus
S. jurei
S. mikatae
S. arboricola
S. kudriavzevii
S. eubayanus
S. uvarum
Population genomics of
Saccharomyces eubayanus
Two of the three big beer families: Skål!
Pale Ale
IPA
Kölsch
Juleøl
Kornøl
Vossaøl
Pilsner
Bayer
Bokkøl
Two of the three big beer families: Skål!
Pale Ale
IPA
Kölsch
Juleøl
Kornøl
Vossaøl
Pilsner
Bayer
Bokkøl
Two of the three big beer families: Skål!
15-25°C
Pale Ale
IPA
Kölsch
Juleøl
Kornøl
Vossaøl
Pilsner
Bayer
Bokkøl
Two of the three big beer families: Skål!
15-25°C
S. cerevisiae
Beer 1
Beer 2
Kveik
Pale Ale
IPA
Kölsch
Juleøl
Kornøl
Vossaøl
Pilsner
Bayer
Bokkøl
Gallone et al 2016
Preiss et al 2018
Two of the three big beer families: Skål!
15-25°C
12-18°C
Stored <7°C
S. cerevisiae
Beer 1
Beer 2
Kveik
Pale Ale
IPA
Kölsch
Juleøl
Kornøl
Vossaøl
Pilsner
Bayer
Bokkøl
Gallone et al 2016
Preiss et al 2018
Two of the three big beer families: Skål!
15-25°C
12-18°C
Stored <7°C
S. cerevisiae
Beer 1
Beer 2
Kveik
Hybrid
Pale Ale
IPA
Kölsch
Juleøl
Kornøl
Vossaøl
Pilsner
Bayer
Bokkøl
Gallone et al 2016
Preiss et al 2018
Libkind et al 2011
Two types of yeasts for two types of Lager
Saaz/Group I Frohberg/Group II
S. pastorianus
x
S. eubayanus S. cerevisiae
Libkind et al 2011
Two types of yeasts for two types of Lager
Saaz/Group I Frohberg/Group II
Hybrid (4n)
Hybrid (3n)
S. carlsbergensis
x
Wendland 2015 Euk Cell
S. eubayanus S. cerevisiae
S. pastorianus
10°C
Maltotriose-
↓Banana flavor
22°C
Maltotriose+
↑Banana flavor
S. eubayanus is distributed worldwide
A. saccharum
F. grandifolia
Nothofagus trees
Pinus taeda
Cedrus spp. Ilex aquifolium
Araucaria araucana
Libkind et al 2011
Bing et al 2014
Peris et al 2014, 2016
Gayevskiy et al 2015
Langdon, Peris et al 2019
Nespolo et al 2019
Cyttaria harioti
Structured populations in S. eubayanus
Peris et al 2014 Mol Ecol
Peris et al 2016 PloS Genetics
Structured populations in S. eubayanus
Peris et al 2014 Mol Ecol
Peris et al 2016 PloS Genetics
Langdon, Peris et al 2019 BioRxiv
Nespolo et al 2019 BioRxiv
yHCT69 yHCT107
yHCT105
yHCT99
yHAB94
CDFM21.L1
yHRVM108
yHKS210
yHAB578
Persistent gene flow
Peris et al 2016 PloS Gen
Persistent gene flow
Peris et al 2016 PloS Gen
Persistent gene flow
Peris et al 2016 PloS Gen
Persistent gene flow
Peris et al 2016 PloS Gen
Langdon, Peris et al 2019 BioRxiv
Nespolo et al 2019 BioRxiv
0.42%
0.58%
0.45%
0.55%
Geographically structured
Geographically structured
Eizaguirre, Peris et al 2019 Env Microbiol
Geographically structured, but also mtDNA haplotypes
Eizaguirre, Peris et al 2019 Env Microbiol
Are Saaz and Frohberg genomes identical?
Peris et al 2016 PloS Gen
None of the S. eubayanus strains is the direct parental donor of lager strains
Peris et al 2016 PloS Gen
Who is the parental S. eubayanus donor?
Langdon, Peris et al 2019 BioRxiv
The Saccharomyces
genus model
S. cerevisiae
S. paradoxus
S. jurei
S. mikatae
S. arboricola
S. kudriavzevii
S. eubayanus
S. uvarum
Population and species range by genetic divergence
Peris et al In preparation
Species range differs between yeasts and multicellular organisms
Peris et al In preparation
The least diverse Saccharomyces species (humans-macaque)
Peris et al In preparation
The most diverse Saccharomyces species (human-birds)
Peris et al In preparation
Saccharomyces strains are phenotypically diverse
Peris et al In preparation
Saccharomyces Genomes 2.0
Peris et al In preparation
Sichuan & West China lineages
What is the source of phylogenetic incongruence?
Most of the incongruence is due to ILS
Peris et al In preparation
Sichuan & West China lineages
Nuclear gene flow mostly limited within species
Gene flow
Peris et al In preparation
How does introgression impact to carbon metabolism?
Kuang et al 2016 eLife
Legras et al 2018 MBE
Peris et al In preparation
Complex ancestries to the GAL/MEL regulon
Peris et al In preparation
Diversity in the galactose metabolism
Peris et al In preparation
Group 1
Group 2
Group 3
Group 4
Group 5
S. cerevisiae
S. paradoxus
S. mikatae
S. kudriavzevii
S. arboricola
S. uvarum
S. eubayanus
Galactose
S. kudriavzevii a special case for galactose study
Peris et al In preparation
Group 1
Group 2
Group 3
Group 4
Group 5
S. cerevisiae
S. paradoxus
S. mikatae
S. kudriavzevii
S. arboricola
S. uvarum
S. eubayanus
Galactose
EU1
Balancing selection of a complete network
Peris et al In preparation
Group 1
Group 2
Group 3
Group 4
Group 5
S. cerevisiae
S. paradoxus
S. mikatae
S. kudriavzevii
S. arboricola
S. uvarum
S. eubayanus
Galactose
Asia A
Asia B
Gene flow promotes loss or gain of a trait
Peris et al In preparation
Group 1
Group 2
Group 3
Group 4
Group 5
S. cerevisiae
S. paradoxus
S. mikatae
S. kudriavzevii
S. arboricola
S. uvarum
S. eubayanus
Galactose
EU2
Two more DNAs
Mitochondrial and 2µm gene flow between species
Gene flow
Mitochondrial
2µm plasmid
Peris et al In preparation
Phenotypic differentiation based on temperature tolerance
Termotolerant
Cryotolerant
Peris et al In preparation
Phenotypic differentiation based on temperature tolerance
Group 1
Group 2
Group 3
Group 4
Group 5
S. cerevisiae
S. paradoxus
S. mikatae
S. kudriavzevii
S. arboricola
S. uvarum
S. eubayanus
Peris et al In preparation
S. cerevisiae
S. paradoxus
S. mikatae
S. jurei
S. kudriavzevii
S. arboricola
S. uvarum
S. eubayanus
Species
Hybridization as a domestication mechanism
Langdon, Peris et al Accepted Nat Ecol & Evol
Peris et al 2018 Yeast
Peris et al 2012a Yeast
Peris et al 2012 BMC Genomics
Peris et al 2012 PloS One
S. cerevisiae
S. paradoxus
S. mikatae
S. jurei
S. kudriavzevii
S. arboricola
S. uvarum
S. eubayanus
Species
94% of interspecies hybrids inherited the non-cerevisiae mtDNA
Langdon, Peris et al Accepted Nat Ecol & Evol
Peris et al 2018 Yeast
Peris et al 2012a Yeast
Peris et al 2012 BMC Genomics
Peris et al 2012 PloS One
60
Mitochondrial inheritance directly related with temperature tolerance
Baker, Peris et al 2019 Sci Adv
Li, Peris et al 2019 Sci Adv
61
Take-home messages
Saccharomyces yeasts are geographically well structured
62
Take-home messages
Saccharomyces yeasts are geographically well structured
Saccharomyces yeasts are diverse
63
Take-home messages
Saccharomyces yeasts are geographically well structured
Saccharomyces yeasts are diverse
Nuclear gene flow is limited between species, but frequent at
the mtDNA and 2µm plasmid
64
Take-home messages
Saccharomyces yeasts are geographically well structured
Saccharomyces yeasts are diverse
Nuclear gene flow is limited between species, but frequent at
the mtDNA and 2µm plasmid
Gene flow can have an impact in the phenotype
65
Take-home messages
Saccharomyces yeasts are geographically well structured
Saccharomyces yeasts are diverse
Nuclear gene flow is limited between species, but frequent at
the mtDNA and 2µm plasmid
Gene flow can have an impact in the phenotype
Mitochondrial inheritance is important to temperature tolerance
66
Take-home messages
Saccharomyces yeasts are geographically well structured
Saccharomyces yeasts are diverse
Nuclear gene flow is limited between species, but frequent at
the mtDNA and 2µm plasmid
Gene flow can have an impact in the phenotype
Mitochondrial inheritance is important to temperature tolerance
The origin of S. eubayanus parental donor of Lager strains is
still unknown
Thank you

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The rise of the yeast genus Saccharomyces: biodiversity and evolution

  • 1. The rise of the yeast genus Saccharomyces: biodiversity and evolution David Peris, Postdoctoral Marie Curie Fellow Biotechnology Department, SBYBI Group (IATA-CSIC) 23th September 2019 @djperis
  • 2. Saccharomyces cerevisiae as a species model Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html Well characterize eukaryotic cell
  • 3. Saccharomyces cerevisiae as a species model Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html Small genome Well characterize eukaryotic cell
  • 4. Saccharomyces cerevisiae as a species model Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html Easy to manipulate Small genome Well characterize eukaryotic cell
  • 5. Saccharomyces cerevisiae as a species model Image provided by: http://faculty.ccbcmd.edu/courses/bio141/lecguide/unit4/fungi/u1fig35.html Easy to manipulate Small genome Similarities to other eukaryotes Well characterize eukaryotic cell
  • 6. S. cerevisiae is important for their multiple applications! Ales Traditional beverages Wine Cider Sake
  • 7. In rich conditions, yeast divides by mitosis Haploid (n) Haploid (n) Diploid (2n) Clonal divisions (mitosis)
  • 8. How do we define a species? Life cycle MAT MATa MAT/MATa Haploid (n) Haploid (n) Diploid (2n) 2 Sexual types (MAT locus)
  • 9. Sexual competent cells can mate MAT MATa MAT/MATa Haploid (n) Haploid (n) Diploid (2n) MAT MATa X MAT/MATa schmoo MATa MAT MATa MAT
  • 10. Sporulation is promoted under starvation or stressful conditions MAT/MATa Diploid (2n)   a a Tetrad Spore Sporulation
  • 11. A diploid gets sexual competent by sporulating MAT/MATa Diploid (2n) MAT MATa X MAT/MATa   a a
  • 12. MAT X MAT/MATa MATa   a a x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x: No growth 4/128 = 3.1% If spore viability below 5% suggests different species (postzygotic barrier) MAT/MATa   a MAT/MATa a   a a
  • 13. Saccharomyces genomes 1.0 S. paradoxus S. mikatae S. kudriavzevii S. uvarum S. cerevisiae Scannell et al 2011
  • 14. The genus Saccharomyces Libkind et al 2011 Liti et al 2013 Naseeb et al 2018 S. paradoxus S. mikatae S. arboricola S. kudriavzevii S. uvarum S. cerevisiae S. eubayanus S. jureii
  • 15. Two stories Population genomics of Saccharomyces eubayanus The Saccharomyces genus as a model S. cerevisiae S. paradoxus S. jurei S. mikatae S. arboricola S. kudriavzevii S. eubayanus S. uvarum
  • 17. Two of the three big beer families: Skål! Pale Ale IPA Kölsch Juleøl Kornøl Vossaøl Pilsner Bayer Bokkøl
  • 18. Two of the three big beer families: Skål! Pale Ale IPA Kölsch Juleøl Kornøl Vossaøl Pilsner Bayer Bokkøl
  • 19. Two of the three big beer families: Skål! 15-25°C Pale Ale IPA Kölsch Juleøl Kornøl Vossaøl Pilsner Bayer Bokkøl
  • 20. Two of the three big beer families: Skål! 15-25°C S. cerevisiae Beer 1 Beer 2 Kveik Pale Ale IPA Kölsch Juleøl Kornøl Vossaøl Pilsner Bayer Bokkøl Gallone et al 2016 Preiss et al 2018
  • 21. Two of the three big beer families: Skål! 15-25°C 12-18°C Stored <7°C S. cerevisiae Beer 1 Beer 2 Kveik Pale Ale IPA Kölsch Juleøl Kornøl Vossaøl Pilsner Bayer Bokkøl Gallone et al 2016 Preiss et al 2018
  • 22. Two of the three big beer families: Skål! 15-25°C 12-18°C Stored <7°C S. cerevisiae Beer 1 Beer 2 Kveik Hybrid Pale Ale IPA Kölsch Juleøl Kornøl Vossaøl Pilsner Bayer Bokkøl Gallone et al 2016 Preiss et al 2018 Libkind et al 2011
  • 23. Two types of yeasts for two types of Lager Saaz/Group I Frohberg/Group II S. pastorianus x S. eubayanus S. cerevisiae Libkind et al 2011
  • 24. Two types of yeasts for two types of Lager Saaz/Group I Frohberg/Group II Hybrid (4n) Hybrid (3n) S. carlsbergensis x Wendland 2015 Euk Cell S. eubayanus S. cerevisiae S. pastorianus 10°C Maltotriose- ↓Banana flavor 22°C Maltotriose+ ↑Banana flavor
  • 25. S. eubayanus is distributed worldwide A. saccharum F. grandifolia Nothofagus trees Pinus taeda Cedrus spp. Ilex aquifolium Araucaria araucana Libkind et al 2011 Bing et al 2014 Peris et al 2014, 2016 Gayevskiy et al 2015 Langdon, Peris et al 2019 Nespolo et al 2019 Cyttaria harioti
  • 26. Structured populations in S. eubayanus Peris et al 2014 Mol Ecol Peris et al 2016 PloS Genetics
  • 27. Structured populations in S. eubayanus Peris et al 2014 Mol Ecol Peris et al 2016 PloS Genetics Langdon, Peris et al 2019 BioRxiv Nespolo et al 2019 BioRxiv yHCT69 yHCT107 yHCT105 yHCT99 yHAB94 CDFM21.L1 yHRVM108 yHKS210 yHAB578
  • 28. Persistent gene flow Peris et al 2016 PloS Gen
  • 29. Persistent gene flow Peris et al 2016 PloS Gen
  • 30. Persistent gene flow Peris et al 2016 PloS Gen
  • 31. Persistent gene flow Peris et al 2016 PloS Gen Langdon, Peris et al 2019 BioRxiv Nespolo et al 2019 BioRxiv 0.42% 0.58% 0.45% 0.55%
  • 34. Geographically structured, but also mtDNA haplotypes Eizaguirre, Peris et al 2019 Env Microbiol
  • 35. Are Saaz and Frohberg genomes identical? Peris et al 2016 PloS Gen
  • 36. None of the S. eubayanus strains is the direct parental donor of lager strains Peris et al 2016 PloS Gen
  • 37. Who is the parental S. eubayanus donor? Langdon, Peris et al 2019 BioRxiv
  • 38. The Saccharomyces genus model S. cerevisiae S. paradoxus S. jurei S. mikatae S. arboricola S. kudriavzevii S. eubayanus S. uvarum
  • 39. Population and species range by genetic divergence Peris et al In preparation
  • 40. Species range differs between yeasts and multicellular organisms Peris et al In preparation
  • 41. The least diverse Saccharomyces species (humans-macaque) Peris et al In preparation
  • 42. The most diverse Saccharomyces species (human-birds) Peris et al In preparation
  • 43. Saccharomyces strains are phenotypically diverse Peris et al In preparation
  • 44. Saccharomyces Genomes 2.0 Peris et al In preparation Sichuan & West China lineages
  • 45. What is the source of phylogenetic incongruence?
  • 46. Most of the incongruence is due to ILS Peris et al In preparation Sichuan & West China lineages
  • 47. Nuclear gene flow mostly limited within species Gene flow Peris et al In preparation
  • 48. How does introgression impact to carbon metabolism? Kuang et al 2016 eLife Legras et al 2018 MBE Peris et al In preparation
  • 49. Complex ancestries to the GAL/MEL regulon Peris et al In preparation
  • 50. Diversity in the galactose metabolism Peris et al In preparation Group 1 Group 2 Group 3 Group 4 Group 5 S. cerevisiae S. paradoxus S. mikatae S. kudriavzevii S. arboricola S. uvarum S. eubayanus Galactose
  • 51. S. kudriavzevii a special case for galactose study Peris et al In preparation Group 1 Group 2 Group 3 Group 4 Group 5 S. cerevisiae S. paradoxus S. mikatae S. kudriavzevii S. arboricola S. uvarum S. eubayanus Galactose EU1
  • 52. Balancing selection of a complete network Peris et al In preparation Group 1 Group 2 Group 3 Group 4 Group 5 S. cerevisiae S. paradoxus S. mikatae S. kudriavzevii S. arboricola S. uvarum S. eubayanus Galactose Asia A Asia B
  • 53. Gene flow promotes loss or gain of a trait Peris et al In preparation Group 1 Group 2 Group 3 Group 4 Group 5 S. cerevisiae S. paradoxus S. mikatae S. kudriavzevii S. arboricola S. uvarum S. eubayanus Galactose EU2
  • 55. Mitochondrial and 2µm gene flow between species Gene flow Mitochondrial 2µm plasmid Peris et al In preparation
  • 56. Phenotypic differentiation based on temperature tolerance Termotolerant Cryotolerant Peris et al In preparation
  • 57. Phenotypic differentiation based on temperature tolerance Group 1 Group 2 Group 3 Group 4 Group 5 S. cerevisiae S. paradoxus S. mikatae S. kudriavzevii S. arboricola S. uvarum S. eubayanus Peris et al In preparation
  • 58. S. cerevisiae S. paradoxus S. mikatae S. jurei S. kudriavzevii S. arboricola S. uvarum S. eubayanus Species Hybridization as a domestication mechanism Langdon, Peris et al Accepted Nat Ecol & Evol Peris et al 2018 Yeast Peris et al 2012a Yeast Peris et al 2012 BMC Genomics Peris et al 2012 PloS One
  • 59. S. cerevisiae S. paradoxus S. mikatae S. jurei S. kudriavzevii S. arboricola S. uvarum S. eubayanus Species 94% of interspecies hybrids inherited the non-cerevisiae mtDNA Langdon, Peris et al Accepted Nat Ecol & Evol Peris et al 2018 Yeast Peris et al 2012a Yeast Peris et al 2012 BMC Genomics Peris et al 2012 PloS One
  • 60. 60 Mitochondrial inheritance directly related with temperature tolerance Baker, Peris et al 2019 Sci Adv Li, Peris et al 2019 Sci Adv
  • 61. 61 Take-home messages Saccharomyces yeasts are geographically well structured
  • 62. 62 Take-home messages Saccharomyces yeasts are geographically well structured Saccharomyces yeasts are diverse
  • 63. 63 Take-home messages Saccharomyces yeasts are geographically well structured Saccharomyces yeasts are diverse Nuclear gene flow is limited between species, but frequent at the mtDNA and 2µm plasmid
  • 64. 64 Take-home messages Saccharomyces yeasts are geographically well structured Saccharomyces yeasts are diverse Nuclear gene flow is limited between species, but frequent at the mtDNA and 2µm plasmid Gene flow can have an impact in the phenotype
  • 65. 65 Take-home messages Saccharomyces yeasts are geographically well structured Saccharomyces yeasts are diverse Nuclear gene flow is limited between species, but frequent at the mtDNA and 2µm plasmid Gene flow can have an impact in the phenotype Mitochondrial inheritance is important to temperature tolerance
  • 66. 66 Take-home messages Saccharomyces yeasts are geographically well structured Saccharomyces yeasts are diverse Nuclear gene flow is limited between species, but frequent at the mtDNA and 2µm plasmid Gene flow can have an impact in the phenotype Mitochondrial inheritance is important to temperature tolerance The origin of S. eubayanus parental donor of Lager strains is still unknown
  • 67.
  • 68.