Applied Microbiology and Biotechnology

, Volume 86, Issue 2, pp 681–691 | Cite as

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

  • Anthony R. Borneman
  • Eveline J. Bartowsky
  • Jane McCarthy
  • Paul J. Chambers
Genomics and Proteomics

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.

Keywords

Comparative genomics Whole genome sequencing Lactic acid bacteria Oenococcus 

Supplementary material

253_2009_2425_MOESM1_ESM.pdf (1 mb)
Online resource 1(PDF 1,024 kb)
253_2009_2425_MOESM2_ESM.pdf (1.1 mb)
Online resource 2(PDF 1173 kb)
253_2009_2425_MOESM3_ESM.xls (76 kb)
Online resource 3(XLS 76 kb)
253_2009_2425_MOESM4_ESM.xls (64 kb)
Online resource 4(XLS 64 kb)
253_2009_2425_MOESM5_ESM.xls (28 kb)
Online resource 5(XLS 28 kb)
253_2009_2425_MOESM6_ESM.xls (406 kb)
Online resource 6(XLS 405 kb)
253_2009_2425_MOESM7_ESM.xls (1004 kb)
Online resource 7(XLS 1004 kb)
253_2009_2425_MOESM8_ESM.xls (351 kb)
Online resource 8(XLS 351 kb)
253_2009_2425_MOESM9_ESM.xls (54 kb)
Online resource 9(XLS 53 kb)

References

  1. Bae S, Fleet GH, Heard GM (2006) Lactic acid bacteria associated with wine grapes from several Australian vineyards. J Appl Microbiol 100:712–727CrossRefGoogle Scholar
  2. Bartowsky EJ, Henschke PA (2004) The ‘buttery’ attribute of wine—diacetyl—desirability, spoilage and beyond. Int J Food Microbiol 96:235–252CrossRefGoogle Scholar
  3. 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 211–233Google Scholar
  4. 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 75:2079–2090CrossRefGoogle Scholar
  5. Bradley RK, Roberts A, Smoot M, Juvekar S, Do J, Dewey C, Holmes I, Pachter L (2009) Fast statistical alignment. PLoS Comp Biol 5:e1000392CrossRefGoogle Scholar
  6. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J (2005) ACT: the Artemis comparison tool. Bioinformatics 21:3422–3423CrossRefGoogle Scholar
  7. Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679CrossRefGoogle Scholar
  8. Dicks LMT, Dellaglio F, Collins MD (1995) Proposal to reclassify Leuconostoc oenos as Oenococcus oeni. Int J Sys Bacteriol 45:395–397CrossRefGoogle Scholar
  9. Duenas M, Irastorza A, Fernandez K, Bilbao A (1995) Heterofermentative Lactobacilli causing ropiness in Basque country ciders. J Food Protect 58:76–80Google Scholar
  10. Garvie EI (1967) Leuconostoc oenos sp. nov. J Gen Microbiol 48:431–438Google Scholar
  11. 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:e43CrossRefGoogle Scholar
  12. 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 33:376–393CrossRefGoogle Scholar
  13. Kelly WJ, Asmundson RV, Hopcroft DH (1989) Growth of Leuconostoc oenos under anaerobic conditions. Am J Enol Vitic 40:277–282Google Scholar
  14. 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 9:179–188CrossRefGoogle Scholar
  15. Lefebure T, Stanhope MJ (2007) Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8:R71CrossRefGoogle Scholar
  16. Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Ant van Leeuw 76:317–331CrossRefGoogle Scholar
  17. MacLean D, Jones JD, Studholme DJ (2009) Application of ‘next-generation’ sequencing technologies to microbial genetics. Nature Rev 7:287–296Google Scholar
  18. 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 103:15611–15616CrossRefGoogle Scholar
  19. Marcobal AM, Sela DA, Wolf YI, Makarova KS, Mills DA (2008) Role of hypermutability in the evolution of the genus Oenococcus. J Bacteriol 190:564–570CrossRefGoogle Scholar
  20. 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 29:465–475CrossRefGoogle Scholar
  21. Nordberg EK (2005) YODA: selecting signature oligonucleotides. Bioinformatics 21:1365–1370CrossRefGoogle Scholar
  22. 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 23:41–46CrossRefGoogle Scholar
  23. 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 74:4703–4710CrossRefGoogle Scholar
  24. 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 11:316–327CrossRefGoogle Scholar
  25. Renouf V, Claisse O, Lonvaud-Funel A (2007) Inventory and monitoring of wine microbial consortia. Appl Microbiol Biot 75:149–164CrossRefGoogle Scholar
  26. 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 411:134–193CrossRefGoogle Scholar
  27. Sarry JE, Gunata Z (2004) Plant and microbial glycoside hydrolases: volatile release from glycosidic aroma precursors. Food Chem 87:509–521CrossRefGoogle Scholar
  28. 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 105:3473–3478CrossRefGoogle Scholar
  29. Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11:472–477CrossRefGoogle Scholar
  30. 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 366:189–199CrossRefGoogle Scholar
  31. Versari A, Parpinello GP, Cattaneo M (1999) Leuconostoc oenos and malolactic fermentation in wine: a review. J Ind Microbiol Biotech 23:447–455CrossRefGoogle Scholar
  32. 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 63:1261–1267Google Scholar
  33. 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 144:1145–1156CrossRefGoogle Scholar
  34. 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 146:3195–3204Google Scholar
  35. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Anthony R. Borneman
    • 1
    • 2
  • Eveline J. Bartowsky
    • 1
  • Jane McCarthy
    • 1
  • Paul J. Chambers
    • 1
  1. 1.The Australian Wine Research InstituteAdelaideAustralia
  2. 2.The Australian Wine Research InstituteAdelaideAustralia

Personalised recommendations