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Biotechnology Letters

, Volume 42, Issue 3, pp 481–492 | Cite as

The effect of some environmental conditions on planktonic growth and biofilm formation by some lactic acid bacteria isolated from a local cheese in Turkey

  • Aylin AkoğluEmail author
Original Research Paper
  • 46 Downloads

Abstract

Objective

The purpose of this study was to determine the effect of some environmental conditions (different temperature degrees and pH values, different salt, glucose and lactose concentrations) on the planktonic growth and biofilm formation ability of the lactic acid bacteria (LAB) isolated from a local cheese in Turkey.

Results

It was determined that Enterococcus lactis EC61 and Enterococcus faecalis EC41 are the most resistant bacteria to the changing environmental conditions and they can stably maintain their planktonic growth in the pH values of 6.5, 7.0, 7.5, and 8.0; in the salt concentrations of 4% and 6.5%; in the glucose concentration of 0.5%; and in the lactose concentrations of 0.5%, 1.5%, and 2.5%. It was found that all strains had the biofilm formation ability and especially the biofilm formation of Enterococcus lactis EC61 and Enterococcus faecalis EC41 strains significantly increased in the acidic pH values and in the increasing glucose and lactose concentrations, and significantly decreased in the increasing salt concentration.

Conclusions

When considered in terms of LAB potential as a starter culture, specifying the effect of some environmental conditions on the planktonic growth and biofilm formation ability is important for the food industry. As a conclusion, it was determined that lactic acid bacteria, which were previously determined to have some starter culture characteristics, had additional properties on the way to being an starter culture.

Keywords

Lactic acid bacteria Starter culture Planktonic growth Biofilm Environmental conditions 

Notes

References

  1. Abdallah M, Benoliel C, Drider D, Dhulster P, Chihib NE (2014) Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Arch Microbiol 196(7):453–472.  https://doi.org/10.1007/s00203-014-0983-1 CrossRefPubMedGoogle Scholar
  2. Akan E, Kınık Ö (2014) Biyofilm oluşum mekanizması ve biyofilmlerin gıda güvenliğine etkisi. J Feed Sci Technol 14:42–51Google Scholar
  3. Akoğlu A, Yaman H, Coşkun H, Sarı H (2017) Isolation, molecular identification and determination of some starter culture properties of lactic acid bacteria isolated from Mengen cheese. SDU J Nat Appl Sci 21(2), 453–459.  https://doi.org/10.19113/sdufbed.11073 CrossRefGoogle Scholar
  4. Borges S, Silva J, Teixeira P (2012) Survival and biofilm formation by Group B streptococci in simulated vaginal fluid at different pHs. Antonie Van Leeuwenhoek 101:677–682.  https://doi.org/10.1007/s10482-011-9666-y CrossRefPubMedGoogle Scholar
  5. Cappitelli F, Polo A, Villa F (2014) Biofilm formation in food processing environments is still poorly understood and controlled. Food Eng Rev 6(1–2):29–42.  https://doi.org/10.1007/s12393-014-9077-8 CrossRefGoogle Scholar
  6. Carpino S, Randazzo CL, Pino A, Russo N, Rapisarda T, Belvedere G, Caggia C (2017) Influence of PDO Ragusano cheese biofilm microbiota on flavour compounds formation. Food Microbiol 61:126–135.  https://doi.org/10.1016/j.fm.2016.09.006 CrossRefPubMedGoogle Scholar
  7. Chen Q, Sa R, Jia J, Xu R (2017) Research on biofilm formation ability of lactic acid bacteria under different conditions. Adv J Food Sci Technol 13(2), 77–82.  https://doi.org/10.19026/ajfst.13.3769 CrossRefGoogle Scholar
  8. Didienne R, Defargues C, Callon C et al (2012) Characteristics of microbial biofilm on wooden vats (‘gerles’) in PDO Salers cheese. Int J Food Microbiol 156:91–101.  https://doi.org/10.1016/j.ijfoodmicro.2012.03.007 CrossRefPubMedGoogle Scholar
  9. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infec Dis 8(9):881–890.  https://doi.org/10.3201/eid0809.020063 CrossRefGoogle Scholar
  10. Elhadidy M, Zahran E (2014) Biofilm mediates Enterococcus faecalis adhesion, invasion and survival into bovine mammary epithelial cells. Lett Appl Microbiol 58:248–254.  https://doi.org/10.1111/lam.12184 CrossRefPubMedGoogle Scholar
  11. Fallah F, Yousefi M, Pourmand MR, Hashemia A, Nazari Alama A, Afshar D (2017) Phenotypic and genotypic study of biofilm formation in enterococci isolated from urinary tract infections. Microb Pathog 108:85–90.  https://doi.org/10.1016/j.micpath.2017.05.014 CrossRefPubMedGoogle Scholar
  12. Fortina MG, Ricci G, Foschino R et al (2007) Phenotypic typing, technological properties and safety aspects of Lactococcus garvieae strains from dairy enviroments. J Appl Microbiol 103:445–453.  https://doi.org/10.1111/j.1365-2672.2006.03265.x CrossRefPubMedGoogle Scholar
  13. Fysun O, Kern H, Wilke B, Langowski HC (2019) Evaluation of factors influencing dairy biofilm formation in filling hoses of food-processing equipment. Food Bioprod Process 113:39–48.  https://doi.org/10.1016/j.fbp.2018.10.009 CrossRefGoogle Scholar
  14. Gavrilova E, Anisimova E, Gabdelkhadieva A et al (2019) Newly isolated lactic acid bacteria from silage targeting biofilms of foodborne pathogens during milk fermentation. BMC Microbiol 19:248.  https://doi.org/10.1186/s12866-019-1618-0 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gómez NC, Ramiro JMP, Quecan BXV, de Melo FBDGB (2016) Use of potential probiotic lactic acid bacteria (LAB) biofilms for the control of Listeria monocytogenes, Salmonella typhimurium, and Escherichia coli O157:H7 biofilms formation. Front Microbiol 7:863.  https://doi.org/10.3389/fmicb.2016.00863 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Herreros MA, Fresno JM, González Prieto MJ, Tornadijo ME (2003) Technological characterization of lactic acid bacteria isolated from Armada cheese (a Spanish goats’ milk cheese). Int Dairy J 13:469–479.  https://doi.org/10.1016/S0958-6946(03)00054-2 CrossRefGoogle Scholar
  17. Kafil HS, Mobarez AM (2015) Assessment of biofilm formation by enterococci isolates from urinary tract infections with different virulence profiles. J King Saud Univ Sci 27(4):312–317.  https://doi.org/10.1016/j.jksus.2014.12.007 CrossRefGoogle Scholar
  18. Kubota H, Senda S, Nomura N, Tokuda H, Uchiyama H (2008) Biofilm formation by lactic acid bacteria and resistance to environmental stress. J Biosci Bioeng 106:381–386.  https://doi.org/10.1263/jbb.106.381 CrossRefPubMedGoogle Scholar
  19. Kubota H, Senda S, Tokuda H, Uchiyama H, Nomura N (2009) Stress resistance of biofilm and planktonic Lactobacillus plantarum subsp. plantarum JCM 1149. Food Microbiol 26:592–597.  https://doi.org/10.1016/j.fm.2009.04.001 CrossRefPubMedGoogle Scholar
  20. Kumar LM, Saad WZ, Mohamad R, Rahim RA (2017) Influence of biofilm-forming lactic acid bacteria against methicillin-resistant Staphylococcus aureus (MRSA S547). Asian Pac J Trop Biomed 7(12):1107–1115.  https://doi.org/10.1016/j.apjtb.2017.10.013 CrossRefGoogle Scholar
  21. Licitra G, Ogier JC, Parayre S et al (2007) Variability of bacterial biofilms of the “tina” wood vats used in the Ragusano cheese-making process. Appl Environ Microbiol 73:6980–6987.  https://doi.org/10.1128/AEM.00835-07 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lortal S, Di Blasi A, Madec MN et al (2009) Tina wooden vat biofilm: a safe and highly efficient lactic acid bacteria delivering system in PDO Ragusano cheese making. Int J Food Microbiol 132:1–8.  https://doi.org/10.1016/j.ijfoodmicro.2009.02.026 CrossRefPubMedGoogle Scholar
  23. Merritt JH, Kadouri DE, O'Toole GA (2005) Growing and analyzing static biofilms. Curr Protoc Microbiol 0(1):1–17.  https://doi.org/10.1002/9780471729259.mc01b01s00 CrossRefGoogle Scholar
  24. Mirkar K, Rawat A, Satish R (2016) Effect of environmental factors on biofilm formation. Indian J Life Sci 5(2):53–64Google Scholar
  25. Mohamed JA, Huang DB (2007) Biofilm formation by enterococci. J Med Microbiol 56:1581–1588.  https://doi.org/10.1099/jmm.0.47331-0 CrossRefPubMedGoogle Scholar
  26. Morandi S, Brasca M, Andrighetto C, Lombardi A, Lodi R (2006) Technological and molecular characterization of enterococci isolated from North West Italian dairy products. Int Dairy J 16:867–875.  https://doi.org/10.1016/j.idairyj.2005.09.005 CrossRefGoogle Scholar
  27. Muruzović M, Mladenović KG, Čomić LR (2018a) In vitro evaluation of resistance to environmental stress by planktonic and biofilm form of lactic acid bacteria isolated from traditionally made cheese from Serbia. Food Biosci 23:54–59.  https://doi.org/10.1016/j.fbio.2018.03.005 CrossRefGoogle Scholar
  28. Muruzović MZ, Mladenović KG, Djilas MD, Stefanović OD, Čomić LR (2018b) In vitro evaluation of antimicrobial potential and ability of biofilm formation of autochthonous Lactobacillus spp. and Lactococcus spp. isolated from traditionally made cheese from Southeastern Serbia. J Food Process Preserv 42:e13776.  https://doi.org/10.1111/jfpp.13776 CrossRefGoogle Scholar
  29. O’Toole GA, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79.  https://doi.org/10.1146/annurev.micro.54.1.49 CrossRefPubMedGoogle Scholar
  30. Percival SL, Malic S, Cruz H, Williams DW (2011) Introduction to biofilms. In: Percival S, Knottenbelt D, Cochrane C (eds) Biofilms and veterinary medicine. Springer, Berlin, pp 41–69CrossRefGoogle Scholar
  31. Piard JC, Briandet R (2015) Lactic acid bacteria biofilms: from their formation to their health and biotechnological potential. In: Mozzi F, Raya RR, Vignolo GM (eds) Biotechnology of Lactic Acid Bacteria: Novel Applications, 2nd edn. Wiley, New York, pp 341–361CrossRefGoogle Scholar
  32. Popović N, Dinić M, Tolinački M et al (2018) New insight into biofilm formation ability, the presence of virulence genes and probiotic potential of Enterococcus sp. dairy isolates. Front Microbiol 9:78.  https://doi.org/10.3389/fmicb.2018.00078 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Rao MS, Pintado J, Stevens WF, Guyot JP (2004) Kinetic growth parameters of different amylolytic and non-amylolytic Lactobacillus strains under different salt and pH conditions. Bioresour Technol 94(3):331–337.  https://doi.org/10.1016/j.biortech.2003.11.028 CrossRefPubMedGoogle Scholar
  34. Salas-Jara MJ, Ilabaca A, Vega M, García A (2016) Biofilm forming Lactobacillus: New challenges for the development of probiotics. Microorganisms 4(3):35.  https://doi.org/10.3390/microorganisms4030035 CrossRefPubMedCentralGoogle Scholar
  35. Somers EB, Johnson ME, Wong ACL (2001) Biofilm formation and contamination of cheese by nonstarter lactic acid bacteria in the dairy environment. J Dairy Sci 84(9):1926–1936.  https://doi.org/10.3168/jds.S0022-0302(01)74634-6 CrossRefPubMedGoogle Scholar
  36. Sun M, Dong J, Xia Y, Shu R (2017) Antibacterial activities of docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) against planktonic and biofilm growing Streptococcus mutans. Microb Pathog 107:212–218.  https://doi.org/10.1016/j.micpath.2017.03.040 CrossRefPubMedGoogle Scholar
  37. Van-de-Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002) Stress responses in lactic acid bacteria. Antonie Van Leeuwenhoek 82:187–216CrossRefGoogle Scholar
  38. Winkelströter LK, Reis Teixeira FB, Silva EP, Alves VF, De Martinis ECP (2014) Unraveling microbial biofilms of importance for food microbiology. Microb Ecol 68:35–46.  https://doi.org/10.1007/s00248-013-0347-4 CrossRefPubMedGoogle Scholar
  39. Yan PF, Liang JP, Jiang YT (2012) The influence of different alkaline pH conditions on Enterococcus faecalis in planktonic and biofilm mode. Shanghai Kou Qiang Yi Xue 21(1):6–8PubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2020

Authors and Affiliations

  1. 1.Department of Nutrition and Dietetics, Faculty of Health SciencesBolu Abant Izzet Baysal UniversityBoluTurkey

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