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Genotypic and phenotypic diversity of Pediococcus pentosaceus strains isolated from food matrices and characterisation of the penocin operon

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Abstract

Lactic acid bacteria (LAB) are widely used in the food industry. Pediococcus spp. belong to the LAB group and include several species that are essential for the quality of fermented food. Pediococcus pentosaceus is the species that is most frequently isolated from fermented food and beverages but its uncontrolled growth during food fermentation processes can contribute to undesired flavours. Hence, the characterisation of these bacteria at the strain level is of great importance for the quality of fermented products. Despite their importance, misidentification at the species level is common for members of the genus Pediococcus. To clarify the taxonomic relationships among strains, a multilocus sequencing approach was developed for the characterisation of a collection of 29 field strains, 1 type strain and 1 reference strain of P. pentosaceus isolated from food. These strains were also tested for several phenotypic properties of technological interest and for the production of bacteriocins. The chromosomal operon involved in the synthesis of the bacteriocin penocin was also investigated. The present study enabled a good genomic characterisation, identifying 17 sequence types, with an overview of phenotypic characteristics related to different technological abilities, and also provides a thorough characterisation of the operon involved in penocin production.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Bisharat N, Cohen DI, Maiden MC, Crook DW, Peto T, Harding RM (2007) The evolution of genetic structure in the marine pathogen, Vibrio vulnificus. Infect Genet Evol 7:685–693

    Article  PubMed  CAS  Google Scholar 

  • Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A (2001) The complete genome sequence of the lactic acid bacterium Lactococcus lactis spp. Lactis IL1403. Genome Res 11:731–753

    Article  PubMed  CAS  Google Scholar 

  • Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681

    Article  PubMed  CAS  Google Scholar 

  • Cai H, Rodriguez BT, Zhang W, Broadbent JR, Steele JL (2007) Genotypic and phenotypic characterization of Lactobacillus casei strains isolated from different ecological niches suggests frequent recombination and niche specificity. Microbiology 153:2655–2665

    Article  PubMed  CAS  Google Scholar 

  • Calmin G, Lefort F, Belbahri L (2008) Multi-loci sequence typing (MLST) for two lacto-acid bacteria (LAB) species: Pediococcus parvulus and P. damnosus. Mol Biotechnol 40:170–179. doi:10.1007/s12033-008-9073-4

    Article  PubMed  CAS  Google Scholar 

  • Campelo AB, Gaspar P, Roces C, Rodríguez A, Kok J, Kuipers OP, Neves AR, Martínez B (2011) The Lcn972 bacteriocin-encoding plasmid pBL1 impairs cellobiose metabolism in Lactococcus lactis. Appl Environ Microbiol 77:7576–7585. doi:10.1128/AEM.06107-11

    Article  PubMed  CAS  Google Scholar 

  • Carraro L, Maifreni M, Bartolomeoli I, Martino ME, Novelli E, Frigo F, Marino M, Cardazzo B (2011) Comparison of culture-dependent and -independent methods for bacterial community monitoring during Montasio cheese manufacturing. Res Microbiol 162:231–239. doi:10.1016/j.resmic.2011.01.002

    Article  PubMed  CAS  Google Scholar 

  • Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM, Beachey EH (1985) Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22:996–1006

    PubMed  CAS  Google Scholar 

  • Coton E, Rollan G, Bertrand A, Lonvaud-Funel A (1998) Histamine producing lactic acid bacteria in wines: early detection, frequency and distribution. Am J Enol Vitic 49:199–204

    CAS  Google Scholar 

  • Dalmış Ü, Soyer A (2008) Effect of processing methods and starter culture (Staphylococcus xylosus and Pediococcus pentosaceus) on proteolytic changes in Turkish sausages (sucuk) during ripening and storage. Meat Sci 80:345–354. doi:10.1016/j.meatsci.2007.12.022

    Article  PubMed  Google Scholar 

  • De Brabandere AG, De Baerdemaeker JG (1999) Effects of process conditions on the pH development during yogurt fermentation. J Food Eng 41:221–227

    Article  Google Scholar 

  • De las Rivas B, Marcobal A, Muñoz R (2004) Allelic diversity and population structure in Oenococcus oeni as determined from sequence analysis of housekeeping genes. Appl Environ Microbiol 70:7210–7219

    Article  PubMed  CAS  Google Scholar 

  • De las Rivas B, Marcobal A, Muñoz R (2006) Development of a multilocus sequence typing method for analysis of Lactobacillus plantarum strains. Microbiology 152:85–93

    Article  PubMed  CAS  Google Scholar 

  • Delétoile A, Passet V, Aires J, Chambaud I, Butel MJ, Smokvina T, Brisse S (2010) Species delineation and clonal diversity in four Bifidobacterium species as revealed by multilocus sequencing. Res Microbiol 161:82–90. doi:10.1016/j.resmic.2009.12.006

    Article  PubMed  Google Scholar 

  • Diancourt L, Passet V, Chervaux C, Garault P, Smokvina T, Brisse S (2007) Multilocus sequence typing of Lactobacillus casei reveals a clonal population structure with low levels of homologous recombination. Appl Environ Microbiol 73:6601–6611

    Article  PubMed  CAS  Google Scholar 

  • Didelot X, Falush D (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251–1266

    Article  PubMed  CAS  Google Scholar 

  • Diep DB, Godager L, Brede D, Nes IF (2006) Data mining and characterization of a novel pediocin-like bacteriocin system from the genome of Pediococcus pentosaceus ATCC 25745. Microbiology 152:1649–1659

    Article  PubMed  CAS  Google Scholar 

  • Dobson CM, Deneer H, Lee S, Hemmingsen S, Glaze S, Ziola B (2002) Phylogenetic analysis of the genus Pediococcus, including Pediococcus claussenii sp. nov., a novel lactic acid bacterium isolated from beer. Int J Syst Evol Microbiol 52:2003–2010

    Article  PubMed  CAS  Google Scholar 

  • Francisco AP, Bugalho M, Ramirez M, Carrico JA (2009) Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinformatics 10:152

    Article  PubMed  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  PubMed  CAS  Google Scholar 

  • Jolley KA, Maiden MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595. doi:10.1186/1471-2105-11-595

    Article  PubMed  Google Scholar 

  • Kjos M, Nes IF, Diep DB (2009) Class II one-peptide bacteriocins target a phylogenetically defined subgroup of mannose phosphotransferase systems on sensitive cells. Microbiology 155:2949–2961. doi:10.1099/mic.0.030015-0

    Article  PubMed  CAS  Google Scholar 

  • Lazzi C, Bove CG, Sgarbi E, Gatti M, La Gioia F, Torriani S, Neviani E (2009) Application of AFLP fingerprint analysis for studying the biodiversity of Streptococcus thermophilus. J Microbiol Meth 79:48–54. doi:10.1016/j.mimet.2009.07.021

    Article  CAS  Google Scholar 

  • Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Tech 15:67–78. doi:10.1016/j.tifs.2003.09.004

    Article  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187

    Article  PubMed  CAS  Google Scholar 

  • Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 95:3140–3145

    Article  PubMed  CAS  Google Scholar 

  • Maifredi M, Marino M, Conte L (2004) Lactic acid fermentation of Brassica rapa: chemical and microbial evaluation of a typical Italian product (brovada). Eur Food Res Technol 218:469–473

    Article  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, Díaz-Muñiz 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 USA 103:15611–15616

    Article  PubMed  Google Scholar 

  • Manca de Nadra MC, Strasser de Saad AM (1995) Polysaccharide production by Pediococcus pentosaceus from wine. Int J Food Microbiol 27:101–106

    Article  PubMed  CAS  Google Scholar 

  • Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262

    Article  PubMed  CAS  Google Scholar 

  • Mora D, Fortina MG, Parini C, Ricci G, Gatti M, Giraffa G, Manachini PL (2002) Genetic diversity and technological properties of Streptococcus thermophilus strains isolated from dairy products. J Appl Microbiol 93:278–287

    Article  PubMed  CAS  Google Scholar 

  • Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primer set. Microbiology 148:257–266

    PubMed  CAS  Google Scholar 

  • Ortu S, Felis GE, Marzotto M, Deriu A, Molicotti P, Sechi LA, Dellaglio F, Zanetti S (2007) Identification and functional characterization of Lactobacillus strains isolated from milk and Gioddu, a traditional Sardinian fermented milk. Int Dairy J 17:1312–1320

    Article  CAS  Google Scholar 

  • Osborne JP, Mira de Orduna R, Pilone G, Liu SQ (2000) Acetaldehyde metabolism by wine lactic acid bacteria. FEMS Microbiol Lett 191:51–55

    Article  PubMed  CAS  Google Scholar 

  • Pereira CS, Santos AJ, Bejerano-Sagie M, Correia PB, Marques JC, Xavier KB (2012) Phosphoenolpyruvate phosphotransferase system regulates detection and processing of the quorum sensing signal autoinducer-2. Mol Microbiol 84:93–104. doi:10.1111/j.1365-2958.2012.08010.x

    Article  PubMed  CAS  Google Scholar 

  • Pfannebecker J, Fröhlich J (2008) Use of a species-specific multiplex PCR for the identification of pediococchi. Int J Food Microbiol 128:288–296. doi:10.1016/j.ijfoodmicro.2008.08.019

    Article  PubMed  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. doi:10.1128/AEM.00132-08

    Article  PubMed  CAS  Google Scholar 

  • Santos EM, Jaime I, Rovira J, Lyhs U, Korkeala H, Björkroth J (2005) Characterization and identification of lactic acid bacteria in “morcilla de Burgos”. Int J Food Microbiol 97:285–296

    Article  PubMed  CAS  Google Scholar 

  • Schillinger U, Lücke F (1989) Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol 55:1901–1906

    PubMed  CAS  Google Scholar 

  • Sharpe ME (1979) Identification of the lactic acid bacteria. In: Skinner FA, Lovelock DW (eds) Identification methods for microbiologists. Academic Press, London, pp 233–259

    Google Scholar 

  • Simpson PJ, Stanton C, Fitzgerald GF, Ross RP (2002) Genomic diversity within the genus Pediococcus as revealed by randomly amplified polymorphic DNA PCR and pulsed-field gel electrophoresis. Appl Environ Microbiol 68:765–771

    Article  PubMed  CAS  Google Scholar 

  • Stiles ME (1996) Biopreservation by lactic acid bacteria. Antonie Van Leeuwenhoek 70:331–345

    Article  PubMed  CAS  Google Scholar 

  • Tanganurat W, Quinquis B, Leelawatcharamas V, Bolotin A (2009) Genotypic and phenotypic characterization of Lactobacillus plantarum strains isolated from Thai fermented fruits and vegetables. J Basic Microbiol 49:377–385. doi:10.1002/jobm.200800185

    Article  PubMed  CAS  Google Scholar 

  • Thomas TD, McKay LL, Morris HA (1985) Lactate metabolism by pediococci isolated from cheese. Appl Environ Microbiol 49:908–913

    PubMed  CAS  Google Scholar 

  • Titgemeyer F, Hillen W (2002) Global control of sugar metabolism: a gram-positive solution. Antonie Van Leeuwenhoek 82:9–71

    Article  Google Scholar 

  • Vos M, Didelot X (2009) A comparison of homologous recombination rates in 805 bacteria and archaea. ISME J 3:199–208. doi:10.1038/ismej.2008.93

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This publication made use of the P. pentosaceus MLST website (http://pubmlst.org/ ppentosaceus/) developed by Keith Jolley and sited at the University of Oxford (Jolley and Maiden 2010). The development of this site has been funded by the Wellcome Trust.

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Correspondence to Maria Elena Martino.

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Martino, M.E., Maifreni, M., Marino, M. et al. Genotypic and phenotypic diversity of Pediococcus pentosaceus strains isolated from food matrices and characterisation of the penocin operon. Antonie van Leeuwenhoek 103, 1149–1163 (2013). https://doi.org/10.1007/s10482-013-9897-1

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