Effect of lactic acid bacteria on Listeria monocytogenes infection and innate immunity in rabbits

https://doi.org/10.17221/247/2019-CJASCitation:Zhao H., Zhang F., Chai J., Wang J. (2020): Effect of lactic acid bacteria on Listeria monocytogenes infection and innate immunity in rabbits. Czech J. Anim. Sci., 65: 23-30.
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The present study aimed to investigate the effect of probiotic lactic acid bacteria (LAB) addition on Listeria monocytogenes translocation and its toxin listeriolysin O (LLO), proinflammatory factors, immune organ indexes and serum immunoglobulins in farmed rabbits. Five treatments included negative control (NC), positive control (PC) with L. monocytogenes infection and supplemental LAB at 3.0 × 106 (low-LAB, L-LAB), 3.0 × 108 (medium-LAB, M-LAB) and 3.0 × 1010 (high-LAB, H-LAB) CFU/kg of diet, respectively. The LAB was a mixture of equal amounts of Lactobacillus acidophilus (ACCC11073), Lactobacillus plantarum (CICC21863) and Enterococcus faecium (CICC20430). A total of 180 weaned rabbits (negative for L. monocytogenes) were randomly assigned to 5 groups with 6 replicates of 6 rabbits each in response to the 5 treatments. L. monocytogenes infection occurred on the first day of feeding trial and dietary LAB supplementation lasted for 14 days. The results showed that on days 7 and 14 post administration, L. monocytogenes in caecum, liver, spleen and lymph nodes was reduced in M-LAB and H-LAB compared to PC (P < 0.05), and linear and quadratic reducing trends were found in liver on day 7 (P ≤ 0.002). On day 14, mucosa LLO mRNA expression and serum TNFα, IL1β and IFNγ were reduced in the three LAB treatments (P < 0.05), and linear and quadratic trends were found on TNFα and IL1β (P ≤ 0.025); indexes of thymus and spleen, serum IgA and IgG were increased in the LAB treatments (P < 0.05). It is concluded that LAB can be used to alleviate L. monocytogenes infection and to improve the immune function of farmed animals.

References:
Arena MP, Silvain A, Normanno G, Grieco F, Drider D, Spano G, Fiocco D. Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front. Microbiol. 2016;7:464.
 
Cavicchioli VQ, Camargo AC, Todorov SD, Nero LA. Potential control of Listeria monocytogenes by bacteriocinogenic Enterococcus hirae ST57ACC and Pediococcus pentosaceus ST65ACC strains isolated from artisanal cheese. Probiotics Antimicrob. Proteins. 2019;11:696-704.
 
Choi HJ, Shin MS, Lee SM, Lee WK. Immunomodulatory properties of Enterococcus faecium JWS 833 isolated from duck intestinal tract and suppression of Listeria monocytogenes infection. Microbiol. Immunol. 2012;56:613-620.
 
Corr SC, Hill C, Gahan CGM. (2009): Understanding the mechanisms by which probiotics inhibit gastrointestinal pathogens. Adv. Food Nutr. Res. 2009;56:1-15.
 
Dalle Zotte A, Szendro Z. The role of rabbit meat as functional food. Meat Sci. 2011;88:319-331. https://doi.org/10.1016/j.meatsci.2011.02.017
 
Ding K, Jiang Q, Wang J, Liu N, Zhang F. Effect of tetramethylpyrazine on growth performance, Campylobacter jejuni carriage and endogenous antimicrobial peptides in rabbits. Czech J. Anim. Sci. 2019a;64:465-471. https://doi.org/10.17221/138/2019-CJAS
 
Ding K, Wang JP, Liu N, Zhang FK. Effect of Artemisia apiacea Hance on growth performance, cecal opportunistic bacteria, and microbicidal peptides in rabbits. Rev. Bras. Zootecn. 2019b;48:e20190118. https://doi.org/10.1590/rbz4820190118
 
Dong Q, Zhang W, Guo L, Niu H, Liu Q, Wang X. Influence of Lactobacillus plantarum individually and in combination with low O2-MAP on the pathogenic potential of Listeria monocytogenes in cabbage. Food Control. 2020;107:106765. https://doi.org/10.1016/j.foodcont.2019.106765
 
Ehsani A, Rezaeiyan A, Hashemi M, Aminzare M, Jannat B, Afshari A. Antibacterial activity and sensory properties of Heracleum persicum essential oil, nisin, and Lactobacillus acidophilus against Listeria monocytogenes in cheese. Vet World. 2019;12:90-96. https://doi.org/10.14202/vetworld.2019.90-96
 
Jiang M, Deng K, Jiang C, Fu M, Guo C, Wang X, Wang X, Meng F, Yang S, Deng K, Chen T, Xin H. Evaluation of the antioxidative, antibacterial, and anti-inflammatory effects of the aloe fermentation supernatant containing Lactobacillus plantarum HM218749.1. Mediators Inflamm. 2016;2016:2945650.
 
Johansson J, Freitag NE. Regulation of Listeria monocytogenes virulence. Microbiol. Spectr. 2019;7:4.
 
Lebeer S, Bron PA, Marco ML, Van Pijkeren JP, O’Connell Motherway M, Hill C, Pot B, Roos S, Klaenhammer T. Identification of probiotic effector molecules: present state and future perspectives. Curr. Opin. Biotechnol. 2018;49:217-223.
 
Liu N, Ru Y, Wang J, Xu T. Effect of dietary sodium phytate and microbial phytase on the lipase activity and lipid metabolism of broiler chickens. Br. J. Nutr. 2010;103:862-868. https://doi.org/10.1017/S0007114509992558
 
Liu N, Deng X, Liang C, Cai H. Effect of broccoli residues fermented with probiotics on the growth performance and health status of broilers challenged with Clostridium perfringens. Rev. Bras. Cienc. Avic. 2018;20:625-631.
 
Lukic J, Jancic I, Mirkovic N, Bufan B, Djokic J, Milenkovic M, Begovic J, Strahinic I, Lozo J. Lactococcus lactis and Lactobacillus salivarius differently modulate early immunological response of Wistar rats co-administered with Listeria monocytogenes. Benef. Microbes. 2017;8:809-822.
 
Meixenberger K, Pache F, Eitel J, Schmeck B, Hippenstiel S, Slevogt H, N’Guessan P, Witzenrath M, Netea MG, Chakraborty T, Suttorp N, Opitz B. Listeria monocytogenes-infected human peripheral blood mononuclear cells produce IL-1beta, depending on listeriolysin O and NLRP3. J. Immunol. 2010;184:922-930. https://doi.org/10.4049/jimmunol.0901346
 
Moslehi-Jenabian S, Vogensen FK, Jespersen L. The quorum sensing luxS gene is induced in Lactobacillus acidophilus NCFM in response to Listeria monocytogenes. Int. J. Food Microbiol. 2011;149:269-273. https://doi.org/10.1016/j.ijfoodmicro.2011.06.011
 
Nguyen BN, Peterson BN, Portnoy DA. Listeriolysin O: a phagosome-specific cytolysin revisited. Cell. Microbiol. 2019;21:e12988. https://doi.org/10.1111/cmi.12988
 
Okamoto M, Nakane A, Minagawa T. Host resistance to an intragastric infection with Listeria monocytogenes in mice depends on cellular immunity and intestinal bacterial flora. Infect. Immun. 1994;62:3080-3085.
 
Osborne SE, Brumell JH. Listeriolysin O: from bazooka to Swiss army knife. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017;372:20160222.
 
Papic B, Golob M, Kusar D, Pate M, Zdovc I. Source tracking on a dairy farm reveals a high occurrence of subclinical mastitis due to hypervirulent Listeria monocytogenes clonal complexes. J. Appl. Microbiol. 2019;127:1349-1361.
 
Popovic N, Djokic J, Brdaric E, Dinic M, Terzic-Vidojevic A, Golic N, Veljovic K. The influence of heat-killed Enterococcus faecium BGPAS1-3 on the tight junction protein expression and immune function in differentiated caco-2 cells infected with Listeria monocytogenes ATCC 19111. Front. Microbiol. 2019;10:412.
 
Puertollano E, Puertollano MA, Cruz-Chamorro L, de Cienfuegos GA, Ruiz-Bravo A, de Pablo MA. Orally administered Lactobacillus plantarum reduces pro-inflammatory interleukin secretion in sera from Listeria monocytogenes infected mice. Br. J. Nutr. 2008;99:819-825. https://doi.org/10.1017/S0007114507832533
 
Radoshevich L, Cossart P. Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis. Nat. Rev. Microbiol. 2018;16:32-46.
 
Regan T, MacSharry J, Brint E. Tracing innate immune defences along the path of Listeria monocytogenes infection. Immunol. Cell Biol. 2014;92:563-569.
 
Riaz A, Noureen S, Liqat I, Arshad M, Arshad N. Antilisterial efficacy of Lactobacillus brevis MF179529 from cow: an in vivo evidence. BMC Complement. Altern. Med. 2019;19:37.
 
Riaz Rajoka MS, Shi J, Zhu J, Shao D, Huang Q, Yang H, Jin M. Capacity of lactic acid bacteria in immunity enhancement and cancer prevention. Appl. Microbiol. Biotechnol. 2016;101:35-45.
 
Rocha KR, Perini HF, de Souza CM, Schueler J, Tosoni NF, Furlaneto MC, Furlaneto-Maia L. Inhibitory effect of bacteriocins from enterococci on developing and preformed biofilms of Listeria monocytogenes, Listeria ivanovii and Listeria innocua. World J. Microbiol. Biotechnol. 2019;35:96.
 
Scaffaro R, Lopresti F, Marino A, Nostro A. Antimicrobial additives for poly(lactic acid) materials and their applications: Current state and perspectives. Appl. Microbiol. Biotechnol. 2018;102:7739-7756.
 
Todorov SD, de Paula OAL, Camargo AC, Lopes DA, Nero LA. Combined effect of bacteriocin produced by Lactobacillus plantarum ST8SH and vancomycin, propolis or EDTA for controlling biofilm development by Listeria monocytogenes. Rev. Argent. Microbiol. 2018;50:48-55.
 
Trabelsi I, Slima SB, Ktari N, Triki M, Abdehedi R, Abaza W, Moussa H, Abdeslam A, Salah RB. Incorporation of probiotic strain in raw minced beef meat: study of textural modification, lipid and protein oxidation and color parameters during refrigerated storage. Meat Sci. 2019;154:29-36. https://doi.org/10.1016/j.meatsci.2019.04.005
 
Vandera E, Lianou A, Kakouri A, Feng J, Koukkou AI, Samelis J. Enhanced control of Listeria monocytogenes by Enterococcus faecium KE82, a multiple enterocin-producing strain, in different milk environments. J. Food Prot. 2017;80:74-85. https://doi.org/10.4315/0362-028X.JFP-16-082
 
Van Zyl WF, Deane SM, Dicks LMT. Enterococcus mundtii ST4SA and Lactobacillus plantarum 423 excludes Listeria monocytogenes from the GIT, as shown by bioluminescent studies in mice. Benef. Microbes. 2016;7:227-235.
 
Wang J, Lin L, Jiang Q, Huang W, Liu N. Probiotics and clay detoxifier protected growth performance and intestinal barrier of lambs fed diets contaminated with aflatoxin B1. Indian J. Anim. Sci. 2019a;89:658-662.
 
Wang J, Lin L, Jiang Q, Huang W, Liu N. Effect of supplemental lactic acid bacteria on the growth performance, glutathione turnover and aflatoxin B1 removal in lambs. Czech J. Anim. Sci. 2019b;64:272-278. https://doi.org/10.17221/5/2019-CJAS
 
Wang J, Lin L, Li B, Zhang F, Liu N. Dietary Artemisia vulgaris meal improved growth performance, gut microbes, and immunity of growing Rex rabbits. Czech J. Anim. Sci. 2019c;64:174-179. https://doi.org/10.17221/162/2018-CJAS
 
Wang J, Liu N, Zhang F. Tetramethylpyrazine protects oxidative stability and gelation property of rabbit myofibrillar proteins. Food Sci. Anim. Resour. 2019d;39:623-631. https://doi.org/10.5851/kosfa.2019.e52
 
Wei X, Zhang Y, Zhou H, Tian F, Ni Y. Antimicrobial activities and in vitro properties of cold-adapted Lactobacillus strains isolated from the intestinal tract of cold water fishes of high latitude water areas in Xinjiang, China. BMC Microbiol. 2019;19:247. https://doi.org/10.1186/s12866-019-1623-3
 
Wery N, Pourcher AM, Stan V, Delgenes JP, Picard-Bonnaud F, Godon JJ. Survival of Listeria monocytogenes and Enterococcus faecium in sludge evaluated by real-time PCR and culture methods. Lett. Appl. Microbiol. 2006;43:131-136.
 
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