Saccharomyces cerevisiae diversity reflects human history

HAL Id: hal-02817929

https://hal.inrae.fr/hal-02817929

Submitted on 6 Jun 2020

HAL is a multi-disciplinary open access

archive for the deposit and dissemination of

sci-entific research documents, whether they are

pub-lished or not. The documents may come from

teaching and research institutions in France or

abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est

destinée au dépôt et à la diffusion de documents

scientifiques de niveau recherche, publiés ou non,

émanant des établissements d’enseignement et de

recherche français ou étrangers, des laboratoires

publics ou privés.

Saccharomyces cerevisiae diversity reflects human

history

Jean Luc Legras, Jean-Marie Cornuet, Francis Karst

To cite this version:

Jean Luc Legras, Jean-Marie Cornuet, Francis Karst. Saccharomyces cerevisiae diversity reflects

human history. 26. International Specialised Symposium on Yeasts, Jun 2007, Sorrento, Italy. 21 p.

�hal-02817929�

SACCHAROMYCES CEREVISIAE DIVERSITY REFLECTS

HUMAN HISTORY

JL Legras , JM Cornuet, & F Karst

Introduction

• Fermented beverages have a special place in our

societies from the economical, cultural and historical

points of view.

• On most continents men have been using fermentation to

produce local alcoholic beverages (rice wine and Sake,

palm wine, wine, beer…).

• Remains of fermented beverages have been found in

China, and dated as -7000 BC.

Vine and Wine making Origin

• The origin of vine

domestication is located in

Caucasus, but the

Spanish Vitis sylvestris

also contributed to actual

vine varieties.

(Mc Govern, 2004

)

• Archeological remains were dated from :

– 5400 BC in Iran (Hajji Firuz Tepe)

– 3150 BC in Egypt (Abydos)

Yeast and fermentations

• What is the importance of History and natural factors

on yeast microflora?

• What are the differences between S. cerevisiae strains

isolated from these fermentations ?

• How diverse are wine strains? at which scale are the

differences noticeable ? (Few vineyards comparison)

Yeast differences

• Several authors have given some information

- Azumi and Goto-Yamamoto, 2001 : AFLP

- Hennequin et al., 2001 : Microsatellites

- Fay and Benavides,2005 : MLST

What are the differences between yeast

from these fermentations ?

Fay et Benavides (2005)

concluded to wine yeast and

sake yeast domestication

because of their lower

diversity compared to wild

yeast

Tested strains (650)

•

Geographic origins :

– Africa, Asia, Australia, Europe (but mainly wine) and America

•

Technological origins :

– Various fermented beverages, cheese and bread

•

Vine and Wine origins :

– different ancient vineyards countries: Europe and Lebanon

– or recent vineyards countries: United States, South Africa

– Most of them were isolated from cellars yet some were from grapes

Evaluation of S. cerevisiae diversity with

Microsatellite typing

Interest of Microsatellite typing:

used for evaluation of the population structure of other yeast (C.

albicans)

Microsatellites

Repeated sequences from 2 to 6 bases :

• (GT)

_n

(GA)

_n

(GC)

_n

(AT)

_n

ou (CAA)

_n

(TAA)

_n

...

(TAAA)n …

• variable number of repeats

• located between two conserved zones

we amplified 12 loci and measured the size of the PCR

fragment

:

• one fragment : homozygosity

Maximum number of alleles detected per locus

Origin

tested

_strains

1 allele

_max

2 alleles

_max

3 alleles

_max

4 alleles

Vine and Wine

Alsace 102

25

57

10

9

Cognac

27

13

13

1

0

Avignon

20

1

16

2

1

Nantes

21

10

9

2

0

Spain

36

9

22

4

1

Austria

17

4

10

2

1

USA

27

11

10

2

4

Cider (Bretagne)

8

2

6

0

0

Beer

18

0

5

7

6

Bread

29

1

7

9

12

Palm Wine (Nigeria)

20

5

7

4

4

Rhum (Antilles)

19

4

7

5

3

China (Miscellaneous)

13

2

5

6

0

DAB117 DAB112 DAB131 DAB115 DAB121 DAB67 P29 6598 COG12 M4Fay Kr756 UHA7 DAB127 LEBI-1.5 ICC99/2TUR

SRC213 SRC147 DAB4 IR2815 IR2627 IR2448 R2323 KL22 IR2601 RA17 IR2217 IR2225 vl3 E5 CY3079 UHA40 UHA9 UHA19 UHA18 VL1

UHA15 LEBI-2.11 LEBI-2.18 ST1-1.18 SH8 MJ43 TA19 COG114 COG106 COG11 MCN10B MCN8B W3 MCN1B MCN10C UHA39 MCN9B DAB59 DAB64 DAB66 IR2679 TA48 UHA8 L2056 ST532 Kr699 Kr740 Kr638 ZIM1901 ZIM1899 b ienFFA KL15 COG105 COG102

c heMIFA IR2194 b ienMIFA DAB111 DAB114 P59 K1-MTF2

IR621 2B1a MJ111 F15 MCN10A Awri796 O ETyp WE372 DAB62 DAB8 UCD2118 ST1-2.20 MCN5B 6281 MCN3B 6664 R3574 IR3137 IR2874 DAB26 DAB56 DAB2 DAB6 DAB13 DAB12 C2C COG126 MJ119 COG115 39503

Mc922 10489hong 6589 10404hong 6333 EDV493 10493hong TA56

1993-esp Kr624 PN8M13 PN1C1 PN3F8 6320 DAB129 DAB137 ST329 KL12 I17 MJ10 MJ38 COG111

MJ48 COG15 COG120 IR2399 PN4F10 10171 Kr743 COG35

COG80 6540 6538 6539 UCD622 UCD624 COGFC10 OC2 LRI-6.3 we14 6346 PN2547 PO5 P10 P21TURC MJ20 UHA33 ST423 R2226 P DBgne 8DBgne 10175 10170 10150 10262

10263 10227 RO400 MCN5C RO402 RO405 MJ54 SRC120 TA02 CogFA5 COG27 ST369 Kr759 UHA16 P astRed ST418 Kr640 UY4

4aPenciu ST414 ST407 1887-esp UCD76 UCD49 COG119 Kr616 c omMIFA KL3 L1414 I37 B94/201 PNC13 IR1993 81Bgne 6ABGne 4D2Bgne UHA11 1W12 1n1d BRG 1994-esp K34 6597 P ABgne Kr648 Kr647 kk6 VitilMO5 TA28

MJ89 MJ123 ST405 ST339 1cPenciu sh3 KL14 Vitilsauv 6227 UHA35 UHA21 ST411 2M4/93 DAB110 SHC11 AWRI350 UHA17 UHA34 PN985 10090 PNC16 SRC237 SRC157 10172 UHA31 UHA29 UHA10

1M1b BM45 UHA30 COG116 COG6

IR1452 TA46 ST421 ST351 Lg'IB28Bdx LC2LTBdx Mc921 UHA36 MJ28 10211 522Davies 6050 UCD623 UCD619 DAB69 Dmontrach DAB63 6400 KL8 CER O EKlos KL19 k d UHA23 6467 UHA20 COG113 COG107 MCN7C MCN8C Kr641 6444

1990-esp 118S SRC270 31348 SRC273 UHA25 UHA27 UHA28 IR2324 IR2050 IR2094 3aPenciu 6aPenciu KL16 UHA13 UHA12 RC212 MCN4C TA13 6579 A2A23 LRI-6.12 A2A8

MJ41 KL20 DAB124 DAB133 COG75 V itCSM MCN7B 6009 PN9830 MCN6A ST336 ST428 ST527 ST520 1A2 07B1a

GE7 56D1a I18

1M8 COG130 UHA24 MCN2A DDII13Bdx DDI12Bdx F10Bdx LgIb1Bdx

MCN7A UHA22 MCN4A MCN9C MCN3C

MCN6C CdeBlancs M30Fay RM11-1a COG28 UHA32 DAB125 COG100 SH7

DAB130 RHST TA10 58Wa2 33gw570 ST522 UCD701 58W3 1896-esp P17 P62 TAO9

1888-esp Kr628 1M1a 6599 3frVal.Cal 6054 1891-esp PO7

1881-esp P54 P37 S TBdx GEI6 GEI8 M13Fay M15Fay

UCD2121 IR2341 IR2702 COG108 MJ112 L oaron UCD2122 MJ14 MJ127 MJ66 MJ88 MJ78 P60 6280 UCD587 CBS5378 E98/4TURC 494 6491 30909 6508 6493 6492 245 228 MJ23 6826 CBS7765 CBS7960 UCD2103 M33Fay KK99/8TURC Y9 TVB1 UCD535 6807

_CBS1907

GEI12 10423hong GEI11 GEI9 UCD580 28640 MJ170 1882-esp 6820 6854 MJ100 c heFFA LR-jura MAA51 c omFFA 10402hong Eg25

CAV21jura 6038 UCD505 2Val.Cal 10422hong 10492hong 10418hong 10419hong YP1 YP2 YQ2 YQ5 YB1 YMG1 YM1 YO3 YC3

YN3 YC2 YC1 Kr645 315 397 CL408 3Val.Cal

YA6 YA2 YL1 YA5 YL2 6345 NL UHA38 hefix1000 YF2 YF1 Cappa1 6662 6663 42920 V itilGY 71B 6464 6465 Primeur 6466 376 KL5 L1515 KL4 KL10 KL7 UCD621 UCD620 309 LEBI-1.18 CBS7958 CBS7957 492 241 CBS7959 460 BeerL7 KROL9 KROL8

BeerL1 CLIB267 BeerL4 CLIB279 BeerL6 BeerL5 UCD916 BeerL2 28756 BeerL3 UCD915 28322 HAE KrOA10 KrOA11 CBS8856 CBS8859 CBS8858 CBS8857

11FCA 52FCA 45FCA 72FCA SLS3 42908 84FCA 16FCA TL230 TL229 63FCA 74FCA 91FCA 89FCA 99FCA 105FCA npa5d1 npa71 NPDR4-7 npa72

npa5a1 Arka npa5b1 NPAB2-2 npa5d2 NPCR4-15 npa21 npa31 npa33 NPCR5-1 NPCR4-14 NPCR2-7 npa61 npa62 npa81 NPAB3-3 fl100 NPAB3-14 CLIB269 CBS400

fl200 W303 FY10 288C FY1679 1885-esp 28711 LV7 Y'IIC11Bdx TVA2 CL414 UCD13 cl219 YPS128 YPS133 CHM 390 236 HS453 HS131 HS361 HS015 HS86 HS668 HS5 HSS YA3 CL409 S hoaXing CL415 LA10 LA12 LA11 CL413

28071 28315 K2 K5 K3 K4 K1 CL411 AWAMORI K11 K7 K9 CL410 K6 CL412 6501

0.2

CBS1171

85

₉₂

46

100

100

46

46

₆₂

100

62

39

100

70

100

77

54

100

46100

92

46

46

46

100

46

54

46

69

39

62

₉₂

92

69

62

69

77

63

92

31

8

Legras et al Mol Ecol 2007

Are Yeast different ?

phenetic tree based on Dc

(Cavalli Sforza 1967)

⇒ Strains are clustered

mainly according to the

technological origin

⇒Specific groups of

related strains

⇒few identical strains

in distant vineyards except

industrial strains

Bread (Italy-Sicily)

Bread (misc.)

Wine

and

Cider

groups

Beer (misc.)

Sake (Japan)

Distillery (China) Rice wine (misc.)

Rum & distillery

(French Indies & Brazil)

Rum & distillery

Fermented milk (France, Morocco)

Palm wine (Nigeria)

Laboratory strains

Details of one group of closely related strains

CIVC 8130

EC1118

=> occurrence of strains identical (or close) to EC1118 or

CIVC8130 in several French or foreign vineyards (

South Africa

,

Austria

(grapes)

, Croatia, Lebanon, Portugal…)

Relationships between strains of the

“Champagne” group

EC1118

8130

Loc3 -1al

KL21

Loc9 +1mot*2

6093

Loc10 et 11Plus 1 al

MJ231a

Loc8 -1al

ST2 1.13

Loc2- 1al

Loc6 +1 motif

ST2 2.14

GAG - 1al

loc11 +1 motif

Loc6 +1 motif

loc3 - 1al

7S

Loc10 -1al

KL1

GAG +1 al

loc11 – 1 al

0030

Loc5 -1al

BV2. 5.6

Loc5 -1al

ST2 2.1

Meiosis and cross ?

UHA14

Meiosis and intratetrad

recombination

Allelic specificity of one group of Bread strains

⇒This suggests that bread yeast are originating from beer

strains and from a second origin that could be a wine yeast.

⇒ Only parasexuality could explain the two alleles from both

origins

Relationships between

groups of strains

Fst genetic distance NJ tree between groups

•

A group of wine yeast separated

from other strains

•

Wine yeast seam to have a unique

origin

•

The position of Lebanon suggest a

Mesopotamia origin .

•

Association between groups show

regional association which

correspond to migration pathways.

•

We find the connection between

0

0,1

0,2

0,3

0,4

0,5

0,6

0,7

0,8

3

4

5

6

7

8

9

10

Logarithm of estimated distance

F

st

/(

1-F

st

)

Correlation between genetic and geographic distances

⇒ link between genetic and geographic distance (r

2

=0.28)

⇒ gene flow

Allelic richness of the different wine origins

Austria

Klost.

Cognac

Geisen

Germ

Firen

Italy

Montp.

Nantes

Rhone

Valley

Romania

Lebanon

Penedes

Spain

Nb

11

26

10

16

19

17

17

8

20

15

GAG 5.9

5.3

4.9

5.7

5.4

6.4

4.2

6.7

6.1

6.3

loc10

5.4

5.1

5.5

5.0

6.1

6.5

6.3

6.2

7.1

8.2

loc11

6.3

5.9

6.2

5.1

5.3

6.1

5.1

7.6

6.5

6.5

loc2

4.1

2.9

2.3

2.8

2.0

3.5

3.1

5.1

4.3

2.9

loc3

3.4

3.7

3.2

4.7

2.1

2.9

2.8

3.6

3.3

3.2

loc4

3.8

3.8

6.4

5.0

4.2

5.4

5.6

5.2

6.8

4.4

loc5

5.8

6.3

6.8

6.6

3.7

7.1

7.7

7.0

6.4

6.8

loc6

3.9

3.3

4.9

3.1

3.6

3.2

2.6

5.5

5.0

3.5

loc7

5.0

4.6

4.5

4.5

3.7

4.1

5.1

5.0

4.9

5.0

loc8

4.8

4.0

4.3

4.4

4.3

4.7

4.5

5.1

4.5

5.2

loc9

1.9

2.1

2.8

1.8

2.7

1.6

2.0

3.6

2.7

3.5

Mean

4.6

4.3

4.7

4.4

3.9

4.7

4.4

5.5

5.3

5.1

Time
Divergence
estimation
between
groups

Bayesian Model ABC (JM CORNUET)

Advantages no mutation rate or number of generations

estimation based on historical hypothesis.

•

The most distant groups are the « Central Europe »

and «Rhône Valley » or Montpellier groups.

Starting Hypothesis :

– Strains are originating from Lebanon or close

– The France/Lebanon divergence dated from 2500

years ago

• => when took place the divergence between

« Lebanon » and « Central Europe » ?

1

2

3

t

₂

t

1

Time
Divergence
estimation
between
groups

• Estimated divergence:

Rhone Valley - Liban :

vs Liban/ « Central Europe»

- 10500 (-4500, -32000)

Montpellier - Liban

vs Liban /«Central Europe»

- 11750 (-4750, -36000)

=> Most probable period posterior

to the last glaciations era

• Number detected alleles per locus show different levels of ploidy

according to the origin of the strains (bread, beer, wine...)

Conclusions

• Yeast strains are specific to the technological origins

• A special cluster for wine strains which suggests a unique origin and

extension that parallels the extension of wine making through history

and can be noticed in the most recent vineyards (USA, South Africa, ...)

• Genetic distances are partially correlated to geographic distances

which suggests several domestications from local flora (Beer,

rice-wine/sake, grape wine, palm wine…)

• The migration of wine yeast started very likely during the Neolithic era

(with wine making?)

• A part of human history also lies in yeast diversity !

Acknowledgments

• Enology

– A. Alais

– F. Karst

– J.L. Legras

– O. Ruh

• Vine genetics

– D. Merdinoglu

– G. Butterlin

– C. Schneider

• Population genetics

– JM Cornuet (CBGP INRA

Montpellier)

•

Strains origin

(Acknowledgments)

–

University of Beyrouth, Liban

–

Weinbau Institut Klosterneuburg, Austria

–

Weinbau Institut, Geisenheim, Germany

–

University of Florence, Italy

–

University of Taragona, Spain

–

NRIB, Japan

–

Stellenbosch University, South Africa

–

U.C. Davis, USA

–

University of Debrecen, Hungary

–

University of Chicago

–

BIV Cognac

–

UHA Colmar

–

ITV Nantes

–

InterRhône Orange

–

INRA UMR SPO Montpellier

–

Clib INA-PG Paris Grignon