The pathogenesis of listeriosis results mainly from the ability of Listeria monocytogenes to attach, invade, replicate and survive within various cell types in mammalian tissues. In this work, the effect of two bacteriocin-producing Carnobacterium (C. divergens V41 and C. maltaromaticum V1) and three non-bacteriocinogenic strains: (C. divergens V41C9, C. divergens 2763, and C. maltaromaticum 2762) was investigated on the reduction of L. monocytogenes Scott A plaque-forming during human infection using the HT-29 in vitro model. All Carnobacteria tested resulted in a reduction in the epithelial cell invasion caused by L. monocytogenes Scott A. To understand better the mechanism underlying the level of L. monocytogenes infection inhibition by Carnobacteria, infection assays from various pretreatments of Carnobacteria were assessed. The results revealed the influence of bacteriocin production combined with a passive mechanism of mammalian cell monolayers protection by Carnobacteria. These initial results showing a reduction in L. monocytogenes virulence on epithelial cells by Carnobacteria would be worthwhile analyzing further as a promising probiotic tool for human health.

Department of Biochemistry and Microbiology Faculty of Food and Biochemical Technology University of Chemistry and Technology Prague Czech Republic

Department of Biochemistry and Microbiology Faculty of Food and Biochemical Technology University of Chemistry and TechnologyPrague Czech Republic; UMR1014 SECALIM INRA OnirisNantes France

UMR1014 SECALIM INRA Oniris Nantes France

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Alemka A., Clyne M., Shanahan F., Tompkins T., Corcionivoschi N., Bourke B. (2010). Probiotic colonization of the adherent mucus layer of HT29MTXE12 cells attenuates Campylobacter jejuni virulence properties. Infect. Immun. 78, 2812–2822. 10.1128/IAI.01249-09 PubMed DOI PMC

Amado I. R., Fuciños C., Fajardo P., Guerra N. P., Pastrana L. (2012). Evaluation of two bacteriocin-producing probiotic lactic acid bacteria as inoculants for controlling Listeria monocytogenes in grass and maize silages. Anim. Feed Sci. Technol. 175, 137–149. 10.1016/j.anifeedsci.2012.05.006 DOI

Beresford M. R., Andrew P. W., Shama G. (2001). Listeria monocytogenes adheres to many materials found in food-processing environments. J. Appl. Microbiol. 90, 1000–1005. 10.1046/j.1365-2672.2001.01330.x PubMed DOI

Bourdichon F., Casaregola S., Farrokh C., Frisvad J. C., Gerds M. L., Hammes W. P., et al. . (2012). Food fermentations: microorganisms with technological beneficial use. Int. J. Food Microbiol. 154, 87–97. 10.1016/j.ijfoodmicro.2011.12.030 PubMed DOI

Brillet A., Pilet M. F., Prévost H., Bouttefroy A., Leroi F. (2004). Biodiversity of Listeria monocytogenes sensitivity to bacteriocin-producing Carnobacterium strains and application in sterile cold-smoked salmon. J. Appl. Microbiol. 97, 1029–1037. 10.1111/j.1365-2672.2004.02383.x PubMed DOI

Brillet A., Pilet M. F., Prévost H., Cardinal M., Leroi F. (2005). Effect of inoculation of Carnobacterium divergens V41, a biopreservative strain against Listeria monocytogenes risk, on the microbiological, chemical and sensory quality of cold-smoked salmon. Int. J. Food Microbiol. 104, 309–324. 10.1016/j.ijfoodmicro.2005.03.012 PubMed DOI

Buchanan R. L., Bagi L. K. (1997). Microbial competition: effect of culture conditions on the suppression of Listeria monocytogenes Scott A by Carnobacterium piscicola. J. Food Prot. 60, 254–261. PubMed

Cleveland J., Montville T. J., Nes I. F., Chikindas M. L. (2001). Bacteriocins: safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 71, 1–20. 10.1016/S0168-1605(01)00560-8 PubMed DOI

Corr S. C., Li Y., Riedel C. U., O'Toole P. W., Hill C., Gahan C. G. (2007). Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc. Natl. Acad. Sci. U.S.A. 104, 7617–7621. 10.1073/pnas.0700440104 PubMed DOI PMC

Devlieghere F., Vermeiren L., Debevere J. (2004). New preservation technologies: possibilities and limitations. Int. Dairy J. 14, 273–285. 10.1016/j.idairyj.2003.07.002 DOI

Douillard F. P., Ribbera A., Kant R., Pietila T. E., Jarvinen H. M., Messing M., et al. . (2013). Comparative genomic and functional analysis of 100 Lactobacillus rhamnosus strains and their comparison with strain GG. PLoS Genet. 9:e1003683. 10.1371/journal.pgen.1003683 PubMed DOI PMC

Duffes F., Leroi F., Boyaval P., Dousset X. (1999). Inhibition of Listeria monocytogenes by Carnobacterium spp. strains in a simulated cold smoked fish system stored at 4°C. Int. J. Food Microbiol. 47, 33–42. 10.1016/S0168-1605(98)00206-2 PubMed DOI

Duodu S., Holst-Jensen A., Skjerdal T., Cappelier J. M., Pilet M. F., Loncarevic S. (2010). Influence of storage temperature on gene expression and virulence potential of Listeria monocytogenes strains grown in a salmon matrix. Food Microbiol. 27, 795–801. 10.1016/j.fm.2010.04.012 PubMed DOI

EFSA (2014). The 2013 updated list of QPS Status recommended biological agents in support of EFSA risk assessments – 1st revision (new additions). EFSA J. 12, 3938.

EFSA ECDC (2015). European food safety authority, European centre for disease prevention and control: the European union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J. 13, 3991.

Ennahar S., Sashihara T., Sonomoto K., Ishizaki A. (2000). Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24, 85–106. 10.1111/j.1574-6976.2000.tb00534.x PubMed DOI

Euzéby J. (1997). List of bacterial names with standing in nomenclature: a folder available on the Internet. Int. J. Syst. Bact. 47, 590–592. 10.1099/00207713-47-2-590 PubMed DOI

Farber J. M., Peterkin P. I. (1991). Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev. 55, 476–511. PubMed PMC

FDA (2015). Generally Recognized as Safe (GRAS) Notifications. Avaliable online at: www.fda.gov/food/ingredientspackaginglabeling/gras/default.htm

Garnier M., Matamoros S., Chevret D., Pilet M. F., Leroi F., Tresse O. (2010). Adaptation to cold and proteomic responses of the psychrotrophic biopreservative Lactococcus piscium strain CNCM I-4031. Appl. Environ. Microbiol. 76, 8011–8018. 10.1128/AEM.01331-10 PubMed DOI PMC

Garriga M., Rubio R., Aymerich T., Ruas-Madiedo P. (2015). Potentially probiotic and bioprotective lactic acid bacteria starter cultures antagonise the Listeria monocytogenes adhesion to HT29 colonocyte-like cells. Benef. Microbes 6, 337–343. 10.3920/BM2014.0056 PubMed DOI

Gildberg A., Johansen A., Bogwald J. (1995). Growth and survival of Atlantic salmon (Salmo salar) fry given diets supplemented with fish protein hydrolysate and lactic acid bacteria during a challenge trial with Aeromonas salmonicida. Aquaculture 138, 23–34. 10.1016/0044-8486(95)01144-7 DOI

Gill H. S., Guarner F. (2004). Probiotics and human health: a clinical perspective. Postgrad. Med. J. 80, 516–526. 10.1136/pgmj.2003.008664 PubMed DOI PMC

Grover S., Rashmi H. M., Srivastava A. K., Batish V. K. (2012). Probiotics for human health -new innovations and emerging trends. Gut. Pathog. 4:15. 10.1186/1757-4749-4-15 PubMed DOI PMC

Guerrieri E., de Niederhäusern S., Messi P., Sabia C., Iseppi R., Anacarso I., et al. (2009). Use of lactic acid bacteria (LAB) biofilms for the control of Listeria monocytogenes in a small-scale model. Food Control 20, 861–865. 10.1016/j.foodcont.2008.11.001 DOI

Guilbaud M., Piveteau P., Desvaux M., Brisse S., Briandet R. (2015). Exploring the diversity of Listeria monocytogenes biofilm architecture by high-throughput confocal laser scanning microscopy and the predominance of the honeycomb-like morphotype. Appl. Environ. Microbiol. 81, 1813–1819. 10.1128/AEM.03173-14 PubMed DOI PMC

Guiral S., Mitchell T. J., Martin B., Claverys J. P. (2005). Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc. Natl. Acad. Sci. U.S.A. 102, 8710–8715. 10.1073/pnas.0500879102 PubMed DOI PMC

Harris L. J., Daeschel M. A., Stiles M. E., Klaenhammer T. R. (1989). Antimicrobial activitz of lactic acid bacteria against Listeria monocytogenes. J. Food Prot. 52, 384–387. PubMed

Johansson M. E., Ambort D., Pelaseyed T., Schutte A., Gustafsson J. K., Ermund A., et al. . (2011). Composition and functional role of the mucus layers in the intestine. Cell. Mol. Life Sci. 68, 3635–3641. 10.1007/s00018-011-0822-3 PubMed DOI PMC

Józefiak D., Sip A., Kaczmarek S., Rutkowski A. (2010). The effects of Carnobacterium divergens AS7 bacteriocin on gastrointestinal microflora in vitro and on nutrient retention in broiler chickens. J. Anim. Feed Sci. 19, 460–467.

Kim K. Y., Frank J. F. (1995). Effects of nutrients on biofilm formation by Listeria monocytogenes on stainless steel. J. Food Prot 58, 24–28. PubMed

Klaenhammer T. R. (2000). Probiotic bacteria: today and tomorrow. J. Nutr. 130, 415–416. PubMed

Koo O., Amalaradjou M., Bhunia A. (2012). Recombinant probiotic expressing Listeria adhesion protein attenuates Listeria monocytogenes virulence in vitro. PLoS ONE 7:e29277. 10.1371/journal.pone.0029277 PubMed DOI PMC

Laukova A., Czikkova S., Laczkova S., Turek P. (1999). Use of enterocin CCM 4231 to control Listeria monocytogenes in experimentally contaminated dry fermented Hornád salami. Int. J. Food Microbiol. 52, 115–119. 10.1016/S0168-1605(99)00125-7 PubMed DOI

Leisner J. J., Hansen M. A., Larsen M. H., Hansen L., Ingmer H., Sorensen S. J. (2012). The genome sequence of the lactic acid bacterium, Carnobacterium maltaromaticum ATCC 35586 encodes potential virulence factors. Int. J. Food Microbiol. 152, 107–115. 10.1016/j.ijfoodmicro.2011.05.012 PubMed DOI

Leisner J. J., Laursen B. G., Prévost H., Drider D., Dalgaard P. (2007). Carnobacterium: positive and negative effects in the environment and in foods. FEMS Microbiol. Rev. 31, 592–613. 10.1111/j.1574-6976.2007.00080.x PubMed DOI PMC

Lesuffleur T., Porchet N., Aubert J. P., Swallow D., Gum J. R., Kim Y. S., et al. . (1993). Differential expression of the human mucin genes MUC1 to MUC5 in relation to growth and differentiation of different mucus-secreting HT-29 cell subpopulations. J. Cell Sci. 106, 771–783. PubMed

Lindgren S. W., Dodrogosz W. J. (1990). Antagonistic activities of lactic acid bacteria in food and feed fermentation. FEMS Microbiol. Rev. 87, 149–164. 10.1111/j.1574-6968.1990.tb04885.x PubMed DOI

Messaoudi S., Madi A., Prévost H., Feuilloley M., Manai M., Dousset X., et al. . (2012). In vitro evaluation of the probiotic potential of Lactobacillus salivarius SMXD51. Anaerobe 18, 584–589. 10.1016/j.anaerobe.2012.10.004 PubMed DOI

Nilsson L., Gram L., Huss H. H. (1999). Growth control of Listeria monocytogenes on cold-smoked salmon using a competitive Lactic Acid Bacteria Flora. J. Food Prot. 62, 336–342. PubMed

Nilsson L., Hansen T. B., Garrido P., Buchrieser C., Glaser P., Knochel S., et al. . (2005). Growth inhibition of Listeria monocytogenes by a nonbacteriocinogenic Carnobacterium pisciola. J. Appl. Microbiol. 98, 172–183. 10.1111/j.1365-2672.2004.02438.x PubMed DOI

Pilchová T., Hernould M., Prévost H., Demnerová K., Pazlarová J., Tresse O. (2014). Influence of food processing environments on structure initiation of static biofilm of Listeria monocytogenes. Food Control 35, 366–372. 10.1016/j.foodcont.2013.07.021 DOI

Pilet M. F., Dousset X., Barré R., Novel G., Desmazeaud M., Piard J. C. (1995). Evidence for two bacteriocins produced by Carnobacterium pisciola and Carnobacterium divergens isolated from fish and active against Listeria monocytogenes. J. Food Prot. 58, 256–262. PubMed

Richard C., Brillet A., Pilet M. F., Prévost H., Drider D. (2003). Evidence on inhibition of Listeria monocytogenes by divercin V41 action. Lett. Appl. Microbiol. 36, 288–292. 10.1046/j.1472-765X.2003.01310.x PubMed DOI

Roche S. M., Velge P., Bottreau E., Durier C., Marquet-van der Mee N., Pardon P. (2001). Assessment of the virulence of Listeria monocytogenes: agreement between a plaque-forming assay with HT-29 cells and infection of immunocompetent mice. Int. J. Food Microbiol. 68, 33–44. 10.1016/S0168-1605(01)00460-3 PubMed DOI

Rocourt J., Jacquet C., Reilly A. (2000). Epidemiology of human listeriosis and seafoods. Int. J. Food Microbiol. 62, 197–209. 10.1016/S0168-1605(00)00336-6 PubMed DOI

Rodriguez E., Tomillo J., Nunez M., Medina M. (1997). Combined effect of bacteriocin-producing lactic acid bacteria and lactoperoxidase system activation on Listeria monocytogenes in refrigerated raw milk. J. Appl. Microbiol. 83, 389–395. 10.1046/j.1365-2672.1997.00243.x PubMed DOI

Sabia C., Manicardi G., Messi P., de Niederhäusern S., Bondi M. (2002). Enterocin 416 K1, an antilisterial bacteriocin produced by Enterococcus casseliflavus IM 416K1 isolated from Italian sausages. Int. J. Food Microbiol. 75, 163–170. 10.1016/S0168-1605(01)00741-3 PubMed DOI

Schöbitz R., Zaror T., León O., Costa M. (1999). A bacteriocin from Carnobacterium pisciola for the control of Listeria monocytogenes in vacuum-packaged meat. Food Microbiol. 16, 249–255. 10.1006/fmic.1998.0241 DOI

Shen T. Y., Qin H. L., Gao Z. G., Fan X. B., Hang X. M., Jiang Y. Q. (2005). [Influences of enteral nutrition combined with probiotics on the gut microecology and barrier function of the rats with abdominal infection]. Zhonghua Wei Chang Wai Ke Za Zhi 8, 443–446. PubMed

Sherman P. M., Johnson-Henry K. C., Yeung H. P., Ngo P. S., Goulet J., Tompkins T. A. (2005). Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect. Immun. 73, 5183–5188. 10.1128/IAI.73.8.5183-5188.2005 PubMed DOI PMC

Shi X., Zhu X. (2009). Biofilm formation and food safety in food industries. Trends Food Sci. Technol. 20, 407–413. 10.1016/j.tifs.2009.01.054 DOI

Srividya D., Prakash S., Dharmesh S., Agrawal R. (2015). Anti-Shigella dysenteriae activity by probiotic lactic acid bacteria (Pediococcus pentosaceus); an in vitro study. J. Microbiol. Biotechnol. Food Sci. 4, 317–320. 10.15414/jmbfs.2015.4.4.317-320 DOI

Swaminathan B., Gerner-Smidt P. (2007). The epidemiology of human listeriosis. Microbes Infect. 9, 1236–1243. 10.1016/j.micinf.2007.05.011 PubMed DOI

Todorov S. D., Furtado D. N., Saad S. M., Tome E., Franco B. D. (2011). Potential beneficial properties of bacteriocin-producing lactic acid bacteria isolated from smoked salmon. J. Appl. Microbiol. 110, 971–986. 10.1111/j.1365-2672.2011.04950.x PubMed DOI

Tresse O., Lebret V., Benezech T., Faille C. (2006). Comparative evaluation of adhesion, surface properties, and surface protein composition of Listeria monocytogenes strains after cultivation at constant pH of 5 and 7. J. Appl. Microbiol. 101, 53–62. 10.1111/j.1365-2672.2006.02968.x PubMed DOI

Tresse O., Shannon K., Pinon A., Malle P., Vialette M., Midelet-Bourdin G. (2007). Variable adhesion of Listeria monocytogenes isolates from food-processing facilities and clinical cases to inert surfaces. J. Food Prot. 70, 1569–1578. PubMed

Turonova H., Briandet R., Rodrigues R., Hernould M., Hayek N., Stintzi A., et al. . (2015). Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions. Front. Microbiol. 6:709. 10.3389/fmicb.2015.00709 PubMed DOI PMC

Tyopponen S., Markkula A., Petaja E., Suihko M. L., Mattila-Sandholm T. (2003). Survival of Listeria monocytogenes in North European type dry sausages fermented by bioprotective meat starter cultures. Food Control 14, 181–185. 10.1016/S0956-7135(02)00086-5 DOI

Vázquez-Boland J. A., Kuhn M., Berche P., Chakraborty T., Domínguez-Bernal G., Goebel W., et al. . (2001). Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14, 584–640. 10.1128/CMR.14.3.584-640.2001 PubMed DOI PMC

Yamazaki K., Suzuki M., Kawai Y. (2003). Inhibition of Listeria monocytogenes in cold-smoked Salmon by Carnobacterium piscicola CS526 isolated from frozen surimi. J. Food Prot. 66, 20–25. PubMed

Zoetendal E. G., von Wright A., Vilpponen-Salmela T., Ben-Amor K., Akkermans A. D., de Vos W. M. (2002). Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl. Environ. Microbiol. 68, 3401–3407. 10.1128/AEM.68.7.3401-3407.2002 PubMed DOI PMC

Within-community variation of interspecific divergence patterns in passerine gut microbiota