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Inhibitory effect of bacteriocins from enterococci on developing and preformed biofilms of Listeria monocytogenes, Listeria ivanovii and Listeria innocua

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Abstract

The biofilm-forming ability of Listeria spp. is a concern to the food industry and health sectors. The aim of this study was to verify the inhibitory activity of bacteriocins produced by enterococci (Enterococcus faecium 20, 22 and 24 and Enterococcus faecalis 27) on developing biofilm and preformed biofilm of Listeria species. Bacteriocins were partially purified from cell free supernatant (CFS). L. monocytogenes 2032, L. innocua 2050 and L. ivanovii 2056 were selected to analyse the inhibitory effect of bacteriocins on biofilm biomass (crystal violet staining) and biofilm viability (XTT-reduction). The biomass of the developing and preformed biofilms of Listeria species were reduced (p < 0.05) in the presence of all bacteriocins tested. Overall, the reduction in biofilm biomass of developing biofilms was up to 87.4% for bacteriocin produced by E. faecium 22 (CFS22) against L. ivanovii and up to 87.1% for CFS22 against L. monocytogenes. These findings are in accordance with those observed in confocal microscopy analysis. Most of the CFS-containing bacteriocin (CFS22, CFS24, CFS27) were effective at decreasing the viability of biofilm cells from all Listeria species. The highest reduction in viability was observed for L. monocytogenes preformed biofilm cells (up to 98.7%), evidenced by fluorescence microscopy of propidium iodide-labelled cells. Scanning electron microscopy showed that cells of biofilm-treated bacteriocins displayed degenerative changes that may be indicative of cellular leakages. This study suggests that bacteriocins produced by enterococci have prospective applications to prevent biofilm formation and/or to reduce cell viability of formed biofilms of distinct Listeria species.

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References

  • Al Atya AK, Belguesmia Y, Chataigne G, Ravallec R, Vachée A, Szunerits S, Boukherroub R, Drider D (2016) Anti-MRSA activities of enterocins DD28 and DD93 and evidences on their role in the inhibition of biofilm formation. Front Microbiol 7:817

    Article  Google Scholar 

  • Alonso B, Cruces R, Pérez A, Sánchez-Carrilo C, Guembe M (2017) Comparison of the XTT and resazurin assay for quantification of the metabolic activity of Staphylococcus aureus biofilm. J Microbiol Methods 139:135–137

    Article  CAS  Google Scholar 

  • Al-Seraih A, Belguesmia Y, Baah J, Szunerits S, Boukherroub R, Drider D (2017) Enterocin B3A–B3B produced by LAB collected from infant faeces: potential utilization in the food industry for Listeria monocytogenes biofilm management. Antonie Van Leeuwenhoek 110:205–219

    Article  CAS  Google Scholar 

  • Alvarez-Ordonez A, Leong D, Morgan CA, Hill C, Gahan CGM, Jordan K (2015) Occurrence, persistence, and virulence potential of Listeria ivanovii in foods and food processing environments in the Republic of Ireland. Biomed Res Int 2015: Article ID 350526

  • Buchanan RL, Gorris LGM, Hayman MM, Jackson TC, Whiting RC (2017) A review of Listeria monocytogenes: an update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control 75:1–13

    Article  Google Scholar 

  • Camargo AC, de Paula OA, Todorov SD, Nero LA (2016) In vitro evaluation of bacteriocins activity against Listeria monocytogenes biofilm formation. Appl Biochem Biotechnol 178:1239–1251

    Article  CAS  Google Scholar 

  • Camargo AC, Todorov SD, Chihib NE, Drider D, Nero LA (2018) Lactic acid bacteria (LAB) and their bacteriocins as alternative biotechnological tools to control Listeria monocytogenes biofilms in food processing facilities. Mol Biotechnol 60:712–726

    Article  CAS  Google Scholar 

  • Chambel L, Sol M, Fernandes I, Barbosa M, Zilhão I, Barata B, Jordan S, Perni S, Shama G, Adrião A, Faleiro L, Requena T, Peláez C, Andrew PW, Tenreiro R (2007) Occurrence and persistence of Listeria spp. in the environment of ewe and cow’s milk cheese dairies in Portugal unveiled by an integrated analysis of identification, typing and spatial-temporal mapping along production cycle. Int J Food Microbiol 116:52–63

    Article  CAS  Google Scholar 

  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745

    Article  CAS  Google Scholar 

  • Cotter PD, Ross RP, Hill C (2013) Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol 11:95–105

    Article  CAS  Google Scholar 

  • den Bakker HC, Cummings CA, Ferreira V, Vatta P, Orsi RH, Degoricija L, Barker M, Petrauskene O, Furtado MR, Wiedmann M (2010) Comparative genomics of the bacterial genus Listeria: genome evolution is characterized by limited gene acquisition and limited gene loss. BMC Genom 11:688

    Article  Google Scholar 

  • EFSA (2017) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J 15:5077

    Google Scholar 

  • Eijsink VG, Skeie M, Middelhoven PH, Brurberg MB, Nes IF (1998) Comparative studies of class IIa bacteriocins of lactic acid bacteria. Appl Environ Microbiol 64:3275–3281

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira V, Wiedmann M, Teixeira P, Stasiewicz MJ (2014) Listeria monocytogenes persistence in food associated environments: epidemiology, strain characteristics, and implications for public health. J Food Prot 77:150–170

    Article  CAS  Google Scholar 

  • Gebretsadik S, Kassa T, Alemayehu H, Huruy K, Kebede N (2011) Isolation and characterization of Listeria monocytogenes and other Listeria species in foods of animal origin in Addis Ababa, Ethiopia. J Infect Public Health 4:22–29

    Article  Google Scholar 

  • Gómez NC, Abriouel H, Grande MJ, Pérez Pulido R, Gálvez A (2012) Effect of enterocin AS-48 in combination with biocides on planktonic and sessile Listeria monocytogenes. Food Microbiol 30:51–58

    Article  Google Scholar 

  • Grosu-Tudor SS, Stancu MM, Pelinescu D, Zamfir M (2014) Characterization of some bacteriocins produced by lactic acid bacteria isolated from fermented foods. World J Microbiol Biotechnol 30:2459–2469

    Article  CAS  Google Scholar 

  • Guillet C, Join-Lambert O, Le Monnier A, Leclercq A, Mechaï F, Mamzer-Bruneel MF, Bielecka MK, Scortti M, Disson O, Berche P, Vazquez-Boland J, Lortholary O, Lecuit M (2010) Human listeriosis caused by Listeria ivanovii. Emerg Infect Dis 16:136–138

    Article  CAS  Google Scholar 

  • Johnson MB, Criss AK (2013) Fluorescence microscopy methods for determining the viability of bacteria in association with mammalian cells. J Vis Exp 79:1–9

    Google Scholar 

  • Mathur H, Field D, Rea MC, Cotter PD, Hill C, Ross RP (2018) Fighting biofilms with lantibiotics and other groups of bacteriocins. NPJ Biofilms Microbiomes 4: Article ID 9

  • Miquel S, Lagrafeuille R, Souweine B, Forestier C (2016) Anti-biofilm activity as a health issue. Front Microbiol 7: Article ID 592

  • Nyenje ME, Green E, Ndip RN (2012) Biofilm formation and adherence characteristics of Listeria ivanovii strains isolated from ready-to-eat foods in Alice, South Africa. Sci World J 2012: Article ID 873909

    Article  Google Scholar 

  • Ogaki MB, Rocha KR, Terra MR, Furlaneto MC, Furlaneto-Maia L (2016) Screening of the enterocin-encoding genes and antimicrobial activity in Enterococcus species. J Microbiol Biotechnol 26:1026–1034

    Article  CAS  Google Scholar 

  • Orgaz B, Puga CH, Martínez-Suárez JV, San Jose C (2013) Biofilm recovery from chitosan action: a possible clue to understand Listeria monocytogenes persistence in food plants. Food Control 32:484–489

    Article  CAS  Google Scholar 

  • Orsi RH, Wiedmann M (2016) Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Appl Microbiol Biotechnol 100:5273–5287

    Article  CAS  Google Scholar 

  • Osman KM, Samir A, Abo-Shama UH, Mohamed EH, Orabi A, Zolnikov T (2016) Determination of virulence and antibiotic resistance pattern of biofilm producing Listeria species isolated from retail raw milk. BMC Microbiol 16:263

    Article  Google Scholar 

  • Pérez-Ibarreche M, Castellano P, Leclercq A, Vignolo G (2016) Control of Listeria monocytogenes biofilms on industrial surfaces by the bacteriocin-producing Lactobacillus sakei CRL1862. FEMS Microbiol Lett 363:fnw118

    Article  Google Scholar 

  • Perrin M, Bemer M, Delamare C (2003) Fatal case of Listeria innocua bacteremia. J Clin Microbiol 41:5308–5309

    Article  Google Scholar 

  • Poimenidou S, Belessi CA, Giaouris ED, Gounadaki AS, Nychas G-JE, Skandamis PN (2009) Listeria monocytogenes attachment to and detachment from stainless steel surfaces in a simulated dairy processing environment. Appl Environ Microbiol 75:7182–7188

    Article  CAS  Google Scholar 

  • Rodríguez-López P, Rodríguez-Herrera JJ, Vázquez-Sánchez D, Cabo ML (2018) Current knowledge on Listeria monocytogenes biofilms in food-related environments: incidence, resistance to biocides, ecology and biocontrol. Foods 7:85

    Article  Google Scholar 

  • Silva CCG, Silva SPM, Ribeiro SC (2018) Application of bacteriocins and protective cultures in dairy food preservation. Front Microbiol 9: Article ID 594

  • Snapir YM, Vaisbein E, Nassar F (2006) Low virulence but potentially fatal outcome-Listeria ivanovii. Eur J Intern Med 17:286–287

    Article  Google Scholar 

  • Vallim DS, Hofer CB, Lisbôa RC, Barbosa AV, Rusak LA, dos Reis CMF, Hofer H (2015) Twenty years of Listeria in Brazil: occurrence of Listeria species and Listeria monocytogenes serovars in food samples in Brazil between 1990 and 2012. BioMed Res Int 2015: Article ID 540204

  • Winkelströter LK, Gomes BC, Thomaz MRS, Souza VM, De Martinis ECP (2011) Lactobacillus sakei 1 and its bacteriocin influence adhesion of Listeria monocytogenes on stainless steel surface. Food Control 22:1404–1407

    Article  Google Scholar 

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Acknowledgements

This work was supported by Fundação Araucária/Governo do Paraná—Brazil, UTFPR-Londrina Campus and PROPPG/State University of Londrina-Parana. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

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Authors and Affiliations

  1. Department of Microbiology, State University of Londrina, Londrina, Paraná, C.P. 6001, 86051990, Brazil

    Kátia Real Rocha, Hugo Felix Perini, Cassia Milena de Souza & Márcia Cristina Furlaneto

  2. Department of Food Technology, Federal Technological University of Paraná, Campus of Londrina-Paraná, Londrina, 86036-370, Brazil

    Janaína Schueler, Natara Favaro Tosoni & Luciana Furlaneto-Maia

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  1. Kátia Real Rocha
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  2. Hugo Felix Perini
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  3. Cassia Milena de Souza
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  4. Janaína Schueler
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  5. Natara Favaro Tosoni
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  6. Márcia Cristina Furlaneto
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  7. Luciana Furlaneto-Maia
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Contributions

KRR, HFP, CMS, JS, NFT carried out the experiments; MCF, LF-M wrote and edited the manuscript; KRR, MCF, LF-M designed the project. All authors read and approved the final manuscript.

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Correspondence to Márcia Cristina Furlaneto or Luciana Furlaneto-Maia.

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Rocha, K.R., Perini, H.F., de Souza, C.M. et al. Inhibitory effect of bacteriocins from enterococci on developing and preformed biofilms of Listeria monocytogenes, Listeria ivanovii and Listeria innocua. World J Microbiol Biotechnol 35, 96 (2019). https://doi.org/10.1007/s11274-019-2675-0

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