Multiple genetic origins of Saccharomyces cerevisiae in bakery

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Multiple genetic origins of Saccharomyces cerevisiae in bakery

Frédéric Bigey, Diego Segond, Lucie Huyghe, Nicolas Agier, Aurélie Bourgais, Anne Friedrich, Delphine Sicard

To cite this version:

Frédéric Bigey, Diego Segond, Lucie Huyghe, Nicolas Agier, Aurélie Bourgais, et al.. Multiple genetic origins of Saccharomyces cerevisiae in bakery. Comparative genomics of eukaryotic microbes: genomes in flux, and flux between genomes, Oct 2019, Sant Feliu de Guixol, Spain. �hal-02950887�

Multiple genetic origins of

Saccharomyces cerevisiae in bakery

Frédéric BIGEY

¹

, Diego SEGOND

¹

, Lucie HUYGHE

^2‡

, Nicolas AGIER

³

, Aurélie BOURGAIS

²

, Anne FRIEDRICH

⁴

, Delphine SICARD

^1*

The origin of bakery strains is polyphyletic. No geographical structuration were found neither for commercial nor for natural sourdough strains. Selection for commercial strains has maintained autotetraploid. Commercial strains are mostly related to strains of the Mixed origin clade on the 1002 genomes tree, which also includes beer strains. Sourdough strains are mosaic and are genetically related to strains from highly diverse environments like human, wine, sake, fruits, tree, soil...

Saccharomyces cerevisiae is an ubiquitous yeast species found in natural and domesticated habitats. It has been domesticated to make a wide diversity of fermented products like wine, sake, beer, cocoa and bread. While bread is of cultural and historical importance, the domestication of S. cerevisiae in bread making is poorly known. Bread can be made either by adding commercial S. cerevisiae strains or by propagating a natural sourdough, which is a mixed of naturally fermented flour, water containing yeast and bacteria. Here we analysed the genetic diversity of 229 S. cerevisiae strains of commercial and sourdough origins to get more insight into bakery yeast domestication.

1 SPO, INRA, Univ. Montpellier, Montpellier SupAgro, Montpellier, France;

2 GQE-Le Moulon, INRA, Univ. Paris-Sud, CNRS, AgroParisTech, Univ. Paris-Saclay, Gif-sur-Yvette, France;

3 LCQB, Sorbonne Université, CNRS, UMR7238, Institut de Biologie Paris-Seine, Paris, France;

4 Université de Strasbourg, CNRS, GMGM, UMR 7156, Strasbourg, France

‡ Present adress: McGill University, Canada

* Correspondence: delphine.sicard@inra.fr

Ploidy analysis of a set of 229 bakery strains. Ploidy was determined using a combination of microsatellites typing (at 15 loci) and cytometry analysis: 31 were commercial yeasts and 198 yeasts were isolated from European sourdoughs in Italy, Belgium and France. A high level of tetraploidy (40%) and aneuploidy (17%) was observed in bakery strains (Table 1). We found that commercial strains were significantly (two sided Fisher’s exact test, p

< 0.005) more tetraploid (68%) than sourdough yeasts (35%). On the other hand, we did not observe any significant difference of ploidy distribution between the 198 sourdough yeasts isolated from Belgium, France and Italy (two sided Fisher’s exact test, p > 0.05, Table 2).

Population structure of 68 diploid bakery strains. Structure was obtained from 33,032 biallelic SNPs from 68 bakery strains using fastStructure. The vertical axis depicts the fractional representation of resolved genetic groups (colors) within each strain (horizontal axis) for K assumed ancestral genetic groups. This analysis yields a population structure in 6 genetic groups with low level of mosaicism.

Genomic phylogenetic tree of 68 diploid bakery strains. Maximum likelyhood phylogenetic tree obtained from 33,032 biallelic SNPs from 68 bakery strains using RAxML (evolution model: GTRGAMMA). The most likely tree from 100 bootstrap replicates was presented. All groups but P3 contains both commercial and sourdough strains. However, groups P3 and P4 are composed mostly of sourdough strains while groups P2 and P6 are composed mostly of commercial strains. No geographical structuration were found neither for commercial nor for sourdough strains.

Table 1 Table 2

Figure 1

Figure 2

LE3

B9c 8 B9b 33

B9b 21

HF3 Pb-25

Pa-2

F-3

Com P-H12 B9b 24

Levante

Com P-H1 1

B9c 3

Tandaco Hirondelle

B9b 39

Rapunzel H-3

Al8

CAPP A

Pb-22

LF5

Lys de France F-13

Al4

B10L-38 B9b 1

1

OF2

IE2

B9c 17 B9b 1

MUCL51221

Al28

B9b 20

NE1

NF2 F-6

B9b 9

F-21

IE1

B9b 6

B9b 35

F-4

GF1

NE2 F-7

B9b 26

QF2

GoldenHome TF2

MUCL51208

AF3 F-12

B10L-36 B10L-13

B10L-31 B9c 16

B9b 29

MUCL51230

CLIB208

B10L-17 B9b 12

B10L-30

YS2

B10L-16 B9b 28

MF2

H-20

Al30 B9b 27

GF3

NF1 OF1

QE1 QE2

Pb-24

MUCL51210 F-9

GoldenField CLIB324

YS4 F-11

B9c 1 1

YS9

B9b 34

Springer

Al39 B9b 18

B9b 3

Pb-18 CLIB215

Al10

Mauripan

Pb-727 F-2

Com MUCL 42920 MUCL52905

MUCL52901

B9c 2

Pa-11

MUCL52906 B9b 5

BE2 DF2

Kolin

Fleischmann B9b 22

Elfin

B9b 37

Pb-38

B9c 4

CE3

Pa-14 Pa-12 B9b 36

TE2

PF5

EF3

Pa-4

H-4 GF2

V-23

MUCL51232

YA3 F-15

CCY -02200-3-

46

B9c 7

MUCL51223

Pb-36

B9c 13

Pa-1

Al20

GF6

NF4

Pb-627 OE3

B10L-15 B9b 23

H-7 B7 13

B9b 32

F-5

Al22

MUCL51219

MUCL51216

B10L-1 B9b 10

B1a 33 Al15

MF1

B5a 12

B14-22

Bioreal F-19

Extra F-8

EF2

B9b 4

FE3

AE2

IF6

MUCL51213

HF2 DF3

B9b 15

RF1

B9c 12 B9c 9

B9b 17

MUCL52909

B9b 7

6464

MUCL51226 H-11 MF3 OE2

MUCL51217

B10L-21

PROUV Y

B9c 10

MUCL51233 F-17

CLIB340

Pb-28 B9b 30

LE1 GF4

B9b 16

Al3 Al18

F-14

H-6

B10L-6 Hirondelle B

9

Pb-17

Finestra Cielo

B9c 1

B9c 14

H-2

SAFR Instant

YQ5

Pb-32 Pb-31

BE1 Pb-29

AE1 B9b 31

B9b 8

Al19 F-20

B9c 15 B9b 38

LF1

EE2

F-10

SBE

MUCL51214 B9b 19

Al36

B10L-8

MUCL51215

MUCL51227

B10L-29

Fermipan FE1

F-16

MUCL51236 F-18

Pb-26 B9b 14

Sequence data RE3

Ploidy

2N 4N

Isolation

commercial sourdough

Population

P1 P2 P3 P4 P6

Tree scale: 0.1

Genetic relatedness of 231 diploid and tetraploid bakery strains. NJ tree calculated from Ritland genetic relatedness (Ritland 1996) calculated from 15 microsatellites loci. The tree shows a clustering concordant with the 6 genomic groups (Figures 1 and 2). Groups P3, P4 are mostly represented by diploid sourdough strains (black squares) while groups P2 and P6 contains mostly commercial tetraploids (white squares).

Figure 3

Distribution of the 68 bakery strains accross the 1002 genomes strains. The clusters defined by structure analysis are in agreement with the clades described in the 1002 genomes project (Peter et al. 2018).

- Group P1 (7 bakery strains) correspond to Wine/europe and Mosaic region 1 clades.

- Group P2 and P6 (23 strains; 7 from sourdough) correspond to Mixed origin clade which also include beer strains, clinical strains, water, fruits, tree leaves and natural islolates. Not distinguished by fastStructure when K equal 4.

- Groups P3 and P4 (19 strains; 16 from sourdough) are located in the Mozaic region 3 and Asian fermentation clades which includes strains isolated from wine, sake, clinical, fermentation, insect, palm wine, fruit, nature, distillery. These two are closely related and were not distinguished by fastStructure when K equal 5

- Group P5 including 3 bakery strains corresponds to African beer cluster.

Figure 4

funded by ANR:

ANR-13-ALID-0005

Mixed origin

Mosaic region 3

African beer Wine/European

0.0 0.2 0.4 0.6 0.8 1.0

0.0 0.2 0.4 0.6 0.8 1.0

0.0 0.2 0.4 0.6 0.8 1.0

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B29_1B29_1B29_1B29_1B29_1B29_1B29_1B29_1 B32_1B32_1B32_1B32_1B32_1B32_1B32_1B32_1

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CLIB340CLIB340CLIB340CLIB340CLIB340CLIB340CLIB340CLIB340 7979797979797979 YS22(E)YS22(E)YS22(E)YS22(E)YS22(E)YS22(E)YS22(E)YS22(E) SBE−1CSBE−1CSBE−1CSBE−1CSBE−1CSBE−1CSBE−1CSBE−1C FleischmannFleischmannFleischmannFleischmannFleischmannFleischmannFleischmannFleischmann YS9YS9YS9YS9YS9YS9YS9YS9 CBS1252CBS1252CBS1252CBS1252CBS1252CBS1252CBS1252CBS1252 64646464646464646464646464646464

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SBDSBDSBDSBDSBDSBDSBDSBD YA3YA3YA3YA3YA3YA3YA3YA3

MUCL51226MUCL51226MUCL51226MUCL51226MUCL51226MUCL51226MUCL51226MUCL51226 CBS1387CBS1387CBS1387CBS1387CBS1387CBS1387CBS1387CBS1387 CBS1428CBS1428CBS1428CBS1428CBS1428CBS1428CBS1428CBS1428

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N34:2−4(a)N34:2−4(a)N34:2−4(a)N34:2−4(a)N34:2−4(a)N34:2−4(a)N34:2−4(a)N34:2−4(a) N26−1−10:7−5(a)N26−1−10:7−5(a)N26−1−10:7−5(a)N26−1−10:7−5(a)N26−1−10:7−5(a)N26−1−10:7−5(a)N26−1−10:7−5(a)N26−1−10:7−5(a) N134:7−1(a)N134:7−1(a)N134:7−1(a)N134:7−1(a)N134:7−1(a)N134:7−1(a)N134:7−1(a)N134:7−1(a)

CLIB318_1CLIB318_1CLIB318_1CLIB318_1CLIB318_1CLIB318_1CLIB318_1CLIB318_1 CLIB324_2CLIB324_2CLIB324_2CLIB324_2CLIB324_2CLIB324_2CLIB324_2CLIB324_2 BruggemanBruggemanBruggemanBruggemanBruggemanBruggemanBruggemanBruggeman

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YS8(E)YS8(E)YS8(E)YS8(E)YS8(E)YS8(E)YS8(E)YS8(E) SD−15SD−15SD−15SD−15SD−15SD−15SD−15SD−15 324−6C324−6C324−6C324−6C324−6C324−6C324−6C324−6C CLIB215CLIB215CLIB215CLIB215CLIB215CLIB215CLIB215CLIB215 CLIB215_3BCLIB215_3BCLIB215_3BCLIB215_3BCLIB215_3BCLIB215_3BCLIB215_3BCLIB215_3B MUCL52901MUCL52901MUCL52901MUCL52901MUCL52901MUCL52901MUCL52901MUCL52901 YS5(E)YS5(E)YS5(E)YS5(E)YS5(E)YS5(E)YS5(E)YS5(E) 319−5C319−5C319−5C319−5C319−5C319−5C319−5C319−5C B16_4B16_4B16_4B16_4B16_4B16_4B16_4B16_4 MUCL42920MUCL42920MUCL42920MUCL42920MUCL42920MUCL42920MUCL42920MUCL42920 YS4YS4YS4YS4YS4YS4YS4YS4 YS11(E)YS11(E)YS11(E)YS11(E)YS11(E)YS11(E)YS11(E)YS11(E) 7777777777777777 CLIB208_1CLIB208_1CLIB208_1CLIB208_1CLIB208_1CLIB208_1CLIB208_1CLIB208_1 CBS1254CBS1254CBS1254CBS1254CBS1254CBS1254CBS1254CBS1254

P1 P2 P3 P4 P5 P6

6 4

5 K

origin ploidy total 2n 4n aneuploidy

commercial 5 21 5 31

sourdough 94 70 34 198 total 99 91 39 229

origin ploidy total 2n 4n aneuploid

France 66 37 26 129

Italy 18 24 7 49

Belgium 10 9 1 20

total 94 70 34 198

SBD

YQ5

MUCL3 0387 CLIB208

-1

319-5 C MUCL51226

MUCL5 1215 AE1 QE1

YS2

CLIB340

MUCL52906

MUCL3 0388

IE1 CBS1

428

CBS1385

CLIB324 -2 CLIB274-1 CBS1

236-a

B16- 4

MUCL51209

Brug geman DBVP

G1058

LE3

MUCL4 2920 B9c-1

SBE -1C

SD-1 5 B29-

1

YS19 RedStar

N134- 7-1a

B9b- 1

YS22 E

CLIB215 B10-1

CLIB192 -1b

N26-1 -10-

7-5a

CBS1 YS8E 387

YS5E CLIB326-1 YS10

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YA3

YS11E

CBS1 254

MUCL5 2901 646-3B YS15

Aline 20 MUCL5

1223

YS20

NF1

CLIB215

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YS9

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Fleischm ann CBS1

252

MUCL51236

324-6 C

B25- 1P N34-2

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YS4

CLIB318 -1 CLIB889

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Microsatellite

Isolation

Commercial Sourdough

Origin Europe

Europe/France Europe/Italy Europe/Belgium Africa

Asia America Oceania NA

Population P1 P2 P3 P4 P5 P6

Mosaic Mosaic

Population P1 P2 P3 P4 P5 P6

Tree scale: 0.1 Isolation

Sourdough Commercial

Mosaic region 1

Asian fermentation