Skip to main content
Log in

Genotypic diversity in Oenococcus oeni by high-density microarray comparative genome hybridization and whole genome sequencing

  • Genomics and Proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Many bacteria display substantial intra-specific genomic diversity that produces significant phenotypic variation between strains of the same species. Understanding the genetic basis of these strain-specific phenotypes is especially important for industrial microorganisms where these characters match individual strains to specific industrial processes. Oenococcus oeni, a bacterium used during winemaking, is one such industrial species where large numbers of strains show significant differences in commercially important industrial phenotypes. To ascertain the basis of these phenotypic differences, the genomic content of ten wine strains of O. oeni were mapped by array-based comparative genome hybridization (aCGH). These strains comprised a genomically diverse group in which large sections of the reference genome were often absent from individual strains. To place the aCGH results in context, whole genome sequence was obtained for one of these strains and compared with two previously sequenced, unrelated strains. While the three strains shared a core group of conserved ORFs, up to 10% of the coding potential of any one strain was specific to that isolate. The genome of O. oeni is therefore likely to be much larger than that present in any single strain and it is these strain-specific regions that are likely to be responsible for differences in industrial phenotypes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bae S, Fleet GH, Heard GM (2006) Lactic acid bacteria associated with wine grapes from several Australian vineyards. J Appl Microbiol 100:712–727

    Article  CAS  Google Scholar 

  • Bartowsky EJ, Henschke PA (2004) The ‘buttery’ attribute of wine—diacetyl—desirability, spoilage and beyond. Int J Food Microbiol 96:235–252

    Article  CAS  Google Scholar 

  • Bartowsky EJ, Pretorius IS (2008) Microbial formation and modification of flavour and off-flavour compounds in wine. In: König H, Unden G, Fröhlich J (eds) Biology of microorganisms on grapes, in must and in wine. Springer, Heidelberg, pp 211–233

    Google Scholar 

  • Bon E, Delaherche A, Bilhere E, De Daruvar A, Lonvaud-Funel A, Le Marrec C (2009) Oenococcus oeni genome plasticity is associated with fitness. App Environ Microbiol 75:2079–2090

    Article  CAS  Google Scholar 

  • Bradley RK, Roberts A, Smoot M, Juvekar S, Do J, Dewey C, Holmes I, Pachter L (2009) Fast statistical alignment. PLoS Comp Biol 5:e1000392

    Article  CAS  Google Scholar 

  • Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J (2005) ACT: the Artemis comparison tool. Bioinformatics 21:3422–3423

    Article  CAS  Google Scholar 

  • Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679

    Article  CAS  Google Scholar 

  • Dicks LMT, Dellaglio F, Collins MD (1995) Proposal to reclassify Leuconostoc oenos as Oenococcus oeni. Int J Sys Bacteriol 45:395–397

    Article  CAS  Google Scholar 

  • Duenas M, Irastorza A, Fernandez K, Bilbao A (1995) Heterofermentative Lactobacilli causing ropiness in Basque country ciders. J Food Protect 58:76–80

    Google Scholar 

  • Garvie EI (1967) Leuconostoc oenos sp. nov. J Gen Microbiol 48:431–438

    CAS  Google Scholar 

  • Gressmann H, Linz B, Ghai R, Pleissner KP, Schlapbach R, Yamaoka Y, Kraft C, Suerbaum S, Meyer TF, Achtman M (2005) Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet 1:e43

    Article  CAS  Google Scholar 

  • Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33:376–393

    Article  CAS  Google Scholar 

  • Kelly WJ, Asmundson RV, Hopcroft DH (1989) Growth of Leuconostoc oenos under anaerobic conditions. Am J Enol Vitic 40:277–282

    Google Scholar 

  • Lang P, Lefebure T, Wang W, Zadoks RN, Schukken Y, Stanhope MJ (2009) Gene content differences across strains of Streptococcus uberis identified using oligonucleotide microarray comparative genomic hybridization. Infect Genet Evol 9:179–188

    Article  CAS  Google Scholar 

  • Lefebure T, Stanhope MJ (2007) Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8:R71

    Article  CAS  Google Scholar 

  • Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Ant van Leeuw 76:317–331

    Article  CAS  Google Scholar 

  • MacLean D, Jones JD, Studholme DJ (2009) Application of ‘next-generation’ sequencing technologies to microbial genetics. Nature Rev 7:287–296

    Google Scholar 

  • Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Diaz-Muniz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O'Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103:15611–15616

    Article  Google Scholar 

  • Marcobal AM, Sela DA, Wolf YI, Makarova KS, Mills DA (2008) Role of hypermutability in the evolution of the genus Oenococcus. J Bacteriol 190:564–570

    Article  CAS  Google Scholar 

  • Mills DA, Rawsthorne H, Parker C, Tamir D, Makarova K (2005) Genomic analysis of Oenococcus oeni PSU-1 and its relevance to winemaking. FEMS Microbiol Rev 29:465–475

    Article  CAS  Google Scholar 

  • Nordberg EK (2005) YODA: selecting signature oligonucleotides. Bioinformatics 21:1365–1370

    Article  CAS  Google Scholar 

  • Pollack JR, Perou CM, Alizadeh AA, Eisen MB, Pergamenschikov A, Williams CF, Jeffrey SS, Botstein D, Brown PO (1999) Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Nature Genet 23:41–46

    Article  CAS  Google Scholar 

  • Rasmussen TB, Danielsen M, Valina O, Garrigues C, Johansen E, Pedersen MB (2008) Streptococcus thermophilus core genome: comparative genome hybridization study of 47 strains. Appl Environ Microbiol 74:4703–4710

    Article  CAS  Google Scholar 

  • Renouf V, Claisse O, Lonvaud-Funel A (2005) Understanding the microbial ecosystem on the grape berry surface through numeration and identification of yeast and bacteria. Aust J Grape Wine Res 11:316–327

    Article  Google Scholar 

  • Renouf V, Claisse O, Lonvaud-Funel A (2007) Inventory and monitoring of wine microbial consortia. Appl Microbiol Biot 75:149–164

    Article  CAS  Google Scholar 

  • Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134–193

    Article  CAS  Google Scholar 

  • Sarry JE, Gunata Z (2004) Plant and microbial glycoside hydrolases: volatile release from glycosidic aroma precursors. Food Chem 87:509–521

    Article  CAS  Google Scholar 

  • Schoen C, Blom J, Claus H, Schramm-Gluck A, Brandt P, Muller T, Goesmann A, Joseph B, Konietzny S, Kurzai O, Schmitt C, Friedrich T, Linke B, Vogel U, Frosch M (2008) Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc Natl Acad Sci U S A 105:3473–3478

    Article  CAS  Google Scholar 

  • Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11:472–477

    Article  CAS  Google Scholar 

  • Trotter M, McAuliffe O, Callanan M, Edwards R, Fitzgerald GF, Coffey A, Ross RP (2006) Genome analysis of the obligately lytic bacteriophage 4268 of Lactococcus lactis provides insight into its adaptable nature. Gene 366:189–199

    Article  CAS  Google Scholar 

  • Versari A, Parpinello GP, Cattaneo M (1999) Leuconostoc oenos and malolactic fermentation in wine: a review. J Ind Microbiol Biotech 23:447–455

    Article  CAS  Google Scholar 

  • Zavaleta AI, Martínez-Murcia AJ, Rodríguez-Valera F (1997) Intraspecific genetic diversity of Oenococcus oeni as derived from DNA fingerprinting and sequence analyses. App Environ Microbiol 63:1261–1267

    CAS  Google Scholar 

  • Ze-Ze L, Teneiro R, Brito L, Santos MA, Paveia H (1998) Physical map of the genome of Oenococcus oeni PSU-1 and localization of genetic markers. Microbiol 144:1145–1156

    Article  CAS  Google Scholar 

  • Ze-Ze L, Teneiro R, Paveia H (2000) The Oenococcus oeni genome: physical and genetic map of strain GM and comparison with the genome of a ‘divergent’ strain, PSU-1. Microbiology 146:3195–3204

    CAS  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The Australian Wine Research Institute (AWRI), a member of the Wine Innovation Cluster in Adelaide, is supported by Australia's grapegrowers and winemakers through their investment body the Grape and Wine Research Development Corporation with matching funding from the Australian Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anthony R. Borneman.

Electronic supplementary material

Online resource 1

(PDF 1,024 kb)

Online resource 2

(PDF 1173 kb)

Online resource 3

(XLS 76 kb)

Online resource 4

(XLS 64 kb)

Online resource 5

(XLS 28 kb)

Online resource 6

(XLS 405 kb)

Online resource 7

(XLS 1004 kb)

Online resource 8

(XLS 351 kb)

Online resource 9

(XLS 53 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borneman, A.R., Bartowsky, E.J., McCarthy, J. et al. Genotypic diversity in Oenococcus oeni by high-density microarray comparative genome hybridization and whole genome sequencing. Appl Microbiol Biotechnol 86, 681–691 (2010). https://doi.org/10.1007/s00253-009-2425-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-009-2425-6

Keywords

Navigation