Role of social wasps in Saccharomyces cerevisiae ecology and evolution

Edited by Nancy A. Moran, Yale University, West Haven, CT, and approved July 5, 2012 (received for review May 18, 2012)
July 30, 2012
109 (33) 13398-13403

Abstract

Saccharomyces cerevisiae is one of the most important model organisms and has been a valuable asset to human civilization. However, despite its extensive use in the last 9,000 y, the existence of a seasonal cycle outside human-made environments has not yet been described. We demonstrate the role of social wasps as vector and natural reservoir of S. cerevisiae during all seasons. We provide experimental evidence that queens of social wasps overwintering as adults (Vespa crabro and Polistes spp.) can harbor yeast cells from autumn to spring and transmit them to their progeny. This result is mirrored by field surveys of the genetic variability of natural strains of yeast. Microsatellites and sequences of a selected set of loci able to recapitulate the yeast strain’s evolutionary history were used to compare 17 environmental wasp isolates with a collection of strains from grapes from the same region and more than 230 strains representing worldwide yeast variation. The wasp isolates fall into subclusters representing the overall ecological and industrial yeast diversity of their geographic origin. Our findings indicate that wasps are a key environmental niche for the evolution of natural S. cerevisiae populations, the dispersion of yeast cells in the environment, and the maintenance of their diversity. The close relatedness of several wasp isolates with grape and wine isolates reflects the crucial role of human activities on yeast population structure, through clonal expansion and selection of specific strains during the biotransformation of fermented foods, followed by dispersal mediated by insects and other animals.

Continue Reading

Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession no. JQ946429–JQ946518).

Acknowledgments

The authors thank Dr. Ramazzotti for useful suggestions on phylogenetic analyses; Mary Forrest for article proofreading; and Prof. L. Bisson (University of California–Davis), Prof. M. Blackwell (Louisiana State University), Dr. S. Jindamorakot (Biotec Culture Collection, Thailand), Prof. C. Kurtzman (ARS culture collection, United States), and Prof. J.P. Sampaio for providing strains. This project was supported by SYBARIS Grant 242220 and by Cantina Isole e Olena grants. Funds for insect culture were provided by the University of Florence.

Supporting Information

Appendix (PDF)
Supporting Information
sd01.xls

References

1
PE McGovern, et al., Fermented beverages of pre- and proto-historic China. Proc Natl Acad Sci USA 101, 17593–17598 (2004).
2
D Cavalieri, PE McGovern, DL Hartl, R Mortimer, M Polsinelli, Evidence for S. cerevisiae fermentation in ancient wine. J Mol Evol 57, S226–S232 (2003).
3
M Teresa Fernández-Espinar, E Barrio, A Querol, Analysis of the genetic variability in the species of the Saccharomyces sensu stricto complex. Yeast 20, 1213–1226 (2003).
4
P Veiga-Crespo, M Poza, M Prieto-Alcedo, TG Villa, Ancient genes of Saccharomyces cerevisiae. Microbiology 150, 2221–2227 (2004).
5
JC Fay, JA Benavides, Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet 1, 66–71 (2005).
6
RK Mortimer, P Romano, G Suzzi, M Polsinelli, Genome renewal: A new phenomenon revealed from a genetic study of 43 strains of Saccharomyces cerevisiae derived from natural fermentation of grape musts. Yeast 10, 1543–1552 (1994).
7
M Polsinelli, P Romano, G Suzzi, R Mortimer, Multiple strains of Saccharomyces cerevisiae on a single grape vine. Lett Appl Microbiol 23, 110–114 (1996).
8
HA Murphy, HA Kuehne, CA Francis, PD Sniegowski, Mate choice assays and mating propensity differences in natural yeast populations. Biol Lett 2, 553–556 (2006).
9
CI Owuama, JR Saunders, Physiological variants of Saccharomyces cerevisiae and Kloeckera apiculata from palm wine and cashew juice. J Appl Bacteriol 68, 491–494 (1990).
10
S Garza, JA Teixidó, V Sanchis, I Viñas, S Condón, Heat resistance of Saccharomyces cerevisiae strains isolated from spoiled peach puree. Int J Food Microbiol 23, 209–213 (1994).
11
FJ Las Heras-Vazquez, L Mingorance-Cazorla, JM Clemente-Jimenez, F Rodriguez-Vico, Identification of yeast species from orange fruit and juice by RFLP and sequence analysis of the 5.8S rRNA gene and the two internal transcribed spacers. FEMS Yeast Res 3, 3–9 (2003).
12
SK Sossou, Y Ameyapoh, SD Karou, C de Souza, Study of pineapple peelings processing into vinegar by biotechnology. Pak J Biol Sci 12, 859–865 (2009).
13
FL Duarte, C Pais, I Spencer-Martins, C Leão, Distinctive electrophoretic isoenzyme profiles in Saccharomyces sensu stricto. Int J Syst Bacteriol 49, 1907–1913 (1999).
14
LK Nyanga, et al., Yeasts and lactic acid bacteria microbiota from masau (Ziziphus mauritiana) fruits and their fermented fruit pulp in Zimbabwe. Int J Food Microbiol 120, 159–166 (2007).
15
M Henselová, D Hudecová, Differences in the microflora of scarified and unscarified seeds of Karwinskia humboldtiana (Rhamnaceae). Folia Microbiol (Praha) 46, 543–548 (2001).
16
IuV Ivannikova, ES Naumova, NN Martynenko, GI Naumov, Characterization of the genome of Saccharomyces yeasts from red berry wines. Mikrobiologiia 76, 225–235 (2007).
17
WF Morrissey, B Davenport, A Querol, AD Dobson, The role of indigenous yeasts in traditional Irish cider fermentations. J Appl Microbiol 97, 647–655 (2004).
18
GI Naumov, ES Naumova, PD Sniegowski, Saccharomyces paradoxus and Saccharomyces cerevisiae are associated with exudates of North American oaks. Can J Microbiol 44, 1045–1050 (1998).
19
GA da Silva, The occurrence of killer, sensitive, and neutral yeasts in Brazilian Riesling Italico grape must and the effect of neutral strains on killing behaviour. Appl Microbiol Biotechnol 46, 112–121 (1996).
20
MJ De La Torre, MC Millan, P Perez-Juan, J Morales, JM Ortega, Indigenous yeasts associated with two Vitis vinifera grape varieties cultured in southern Spain. Microbios 100, 27–40 (1999).
21
I Masneuf, J Hansen, C Groth, J Piskur, D Dubourdieu, New hybrids between Saccharomyces sensu stricto yeast species found among wine and cider production strains. Appl Environ Microbiol 64, 3887–3892 (1998).
22
C Nurgel, H Erten, A Canbaş, T Cabaroğlu, S Selli, Influence of Saccharomyces cerevisiae strains on fermentation and flavor compounds of white wines made from cv. Emir grown in Central Anatolia, Turkey. J Ind Microbiol Biotechnol 29, 28–33 (2002).
23
R Mortimer, M Polsinelli, On the origins of wine yeast. Res Microbiol 150, 199–204 (1999).
24
D Schuller, M Casal, The genetic structure of fermentative vineyard-associated Saccharomyces cerevisiae populations revealed by microsatellite analysis. Antonie van Leeuwenhoek 91, 137–150 (2007).
25
MR Goddard, N Anfang, R Tang, RC Gardner, C Jun, A distinct population of Saccharomyces cerevisiae in New Zealand: Evidence for local dispersal by insects and human-aided global dispersal in oak barrels. Environ Microbiol 12, 63–73 (2010).
26
N Francesca, DE Canale, L Settanni, G Moschetti, Dissemination of wine-related yeasts by migratory birds. Envir Microbiol Rep 4, 105–112 (2012).
27
AM El-Tabey Award Shihata, EM Mrak, Intestinal yeast floras of successive population of Drosophila. Evolution 6, 325–332 (1952).
28
RK Mortimer, Evolution and variation of the yeast (Saccharomyces) genome. Genome Res 10, 403–409 (2000).
29
H Phaff The Life of Yeasts: Their Nature, Activity, Ecology, and Relation to Mankind (Harvard Univ Press, Cambridge, 2000).
30
S Stevic, The significance of bees (Apis sp.) and wasps (Vespa sp.) as carriers of yeast for the microflora of grapes and the quality of wine. Arkhiv Poljjoprivredna Nauke 50, 80–92 (1962).
31
A Basukriadi, W Sjamsuridzal, BB Putra, Molecular identification and diversity of yeasts associated with Apis cerana foraging on flowers of Jatropha integerrima. Microbiol Indones 4, 44–48 (2010).
32
M Gilliam, LJ Wickerham, HL Morton, RD Martin, Yeasts isolated from honey bees, Apis mellifera, fed 2,4-D and antibiotics. J Invertebr Pathol 24, 349–356 (1974).
33
JL Legras, O Ruh, D Merdinoglu, F Karst, Selection of hypervariable microsatellite loci for the characterization of Saccharomyces cerevisiae strains. Int J Food Microbiol 102, 73–83 (2005).
34
M Ramazzotti, L Berná, I Stefanini, D Cavalieri, A computational pipeline to discover highly phylogenetically informative genes in sequenced genomes: Application to Saccharomyces cerevisiae natural strains. Nucleic Acids Res 40, 3834–3848 (2012).
35
G Liti, et al., Population genomics of domestic and wild yeasts. Nature 458, 337–341 (2009).
36
C Erny, et al., Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the northern european wine-making environment. Appl Environ Microbiol 78, 3256–3265 (2012).
37
M Sipiczki, Interspecies hybridization and recombination in Saccharomyces wine yeasts. FEMS Yeast Res 8, 996–1007 (2008).
38
HM Daniel, et al., Yeast diversity of Ghanaian cocoa bean heap fermentations. FEMS Yeast Res 9, 774–783 (2009).
39
M Combina, et al., Yeasts associated to Malbec grape berries from Mendoza, Argentina. J Appl Microbiol 98, 1055–1061 (2005).
40
S Stevic, The significance of bees (Apis sp.) and wasps (Vespa sp.) as carriers of yeast for the microflora of grapes and the quality of wine. Arkhiv. Poljjoprivredne Nauke 50, 80–92 (1962).
41
D Schuller, et al., Genetic characterization of commercial Saccharomyces cerevisiae isolates recovered from vineyard environments. Yeast 24, 625–636 (2007).
42
E Valero, D Schuller, B Cambon, M Casal, S Dequin, Dissemination and survival of commercial wine yeast in the vineyard: A large-scale, three-years study. FEMS Yeast Res 5, 959–969 (2005).
43
G Cordero-Bueso, T Arroyo, A Serrano, E Valero, Remanence and survival of commercial yeast in different ecological niches of the vineyard. FEMS Microbiol Ecol 77, 429–437 (2011).
44
MD Rose, F Winston, P Hieter Methods in Yeast Genetics (Cold Spring Harbor, New York, 1990).
45
F Sebastiani, C Barberio, E Casalone, D Cavalieri, M Polsinelli, Crosses between Saccharomyces cerevisiae and Saccharomyces bayanus generate fertile hybrids. Res Microbiol 153, 53–58 (2002).
46
S Dray, AB Dufour, The ade4 package: Implementing the duality diagram for ecologists. J Stat Softw 22, 1–20 (2007).
47
JM Cherry, et al., Saccharomyces Genome Database: The genomics resource of budding yeast. Nucleic Acids Rest 40, D700–D705 (2012).
48
JK Pritchard, M Stephens, NA Rosenberg, P Donnelly, Association mapping in structured populations. Am J Hum Genet 67, 170–181 (2000).
49
M Jakobsson, NA Rosenberg, CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806 (2007).
50
JL Legras, D Merdinoglu, JM Cornuet, F Karst, Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol Ecol 16, 2091–2102 (2007).
51
LL Cavalli-Sforza, AW Edwards, Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19, 233–257 (1967).
52
K Tamura, et al., MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731–2739 (2011).
53
H Gao, S Williamson, CD Bustamante, A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176, 1635–1651 (2007).
54
NA Rosenberg, Distruct: A program for the graphical display of population structure. Mol Ecol Notes 4, 137–138 (2004).
55
J Liang, et al., Study the oxidative injury of yeast cells by NADH autofluorescence. Spectrochim Acta A Mol Biomol Spectrosc 67, 355–359 (2007).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 109 | No. 33
August 14, 2012
PubMed: 22847440

Classifications

Data Availability

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession no. JQ946429–JQ946518).

Submission history

Published online: July 30, 2012
Published in issue: August 14, 2012

Keywords

  1. evolutionary biology
  2. genomics

Acknowledgments

The authors thank Dr. Ramazzotti for useful suggestions on phylogenetic analyses; Mary Forrest for article proofreading; and Prof. L. Bisson (University of California–Davis), Prof. M. Blackwell (Louisiana State University), Dr. S. Jindamorakot (Biotec Culture Collection, Thailand), Prof. C. Kurtzman (ARS culture collection, United States), and Prof. J.P. Sampaio for providing strains. This project was supported by SYBARIS Grant 242220 and by Cantina Isole e Olena grants. Funds for insect culture were provided by the University of Florence.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Irene Stefanini1
Dipartimento di Farmacologia, University of Florence, 50139, Florence, Italy;
Leonardo Dapporto1
Dipartimento di Biologia Evoluzionistica, University of Florence, 50125, Florence, Italy;
Dipartimento di Biotecnologie Agrarie, University of Florence, 50144, Florence, Italy;
Jean-Luc Legras
INRA (Institut National de la Recherche Agronomique), UMR1083 (Unité Mixte de Recherche Sciences pour l'Oenologie), F-34060 Montpellier, France;
Montpellier SupAgro, UMR1083 (Unité Mixte de Recherche Sciences pour l'Oenologie), F-34060 Montpellier, France;
Université Montpellier I, UMR1083 (Unité Mixte de Recherche Sciences pour l'Oenologie), F-34060 Montpellier, France;
Antonio Calabretta
Dipartimento di Farmacologia, University of Florence, 50139, Florence, Italy;
Dipartimento di Biologia Evoluzionistica, University of Florence, 50125, Florence, Italy;
Monica Di Paola
Dipartimento di Scienze per la Salute della Donna e del Bambino, Ospedale Pediatrico Meyer, University of Florence, 50139, Florence, Italy;
Carlotta De Filippo
Centre for Research and Innovation, Fondazione Edmund Mach, Via E. Mach 1, 38010 San Michele all'Adige, Trento, Italy; and
Roberto Viola
Centre for Research and Innovation, Fondazione Edmund Mach, Via E. Mach 1, 38010 San Michele all'Adige, Trento, Italy; and
Paolo Capretti
Dipartimento di Biotecnologie Agrarie, University of Florence, 50144, Florence, Italy;
Mario Polsinelli
Dipartimento di Biologia Evoluzionistica, University of Florence, 50125, Florence, Italy;
Stefano Turillazzi
Dipartimento di Biologia Evoluzionistica, University of Florence, 50125, Florence, Italy;
Centro di Servizi di Spettromeria di Massa, University of Florence, Florence, Italy
Duccio Cavalieri2 [email protected]
Dipartimento di Farmacologia, University of Florence, 50139, Florence, Italy;
Centre for Research and Innovation, Fondazione Edmund Mach, Via E. Mach 1, 38010 San Michele all'Adige, Trento, Italy; and

Notes

2
To whom correspondence should be addressed. E-mail: [email protected].
Author contributions: M.P., S.T., and D.C. designed research; I.S., L.D., J.-L.L., A.C., M.D.P., C.D.F., and D.C. performed research; I.S., L.D., J.-L.L., A.C., M.D.P., C.D.F., R.V., P.C., M.P., S.T., and D.C. analyzed data; and I.S., L.D., and D.C. wrote the paper.
1
I.S. and L.D. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to get full access to it.

    Single Article Purchase

    Role of social wasps in Saccharomyces cerevisiae ecology and evolution
    Proceedings of the National Academy of Sciences
    • Vol. 109
    • No. 33
    • pp. 13133-13464

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media