Probiotic Limosilactobacillus reuteri KUB-AC5 inhibits growth of clinical Salmonella enterica typhimurium isolates
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Abstract
Salmonella enterica Typhimurium (STM) is a causative agent of an important foodborne disease, non-typhoidal salmonellosis (NTS). Although NTS causes self-limiting acute diarrhea in a healthy host, it can result in a life-threatening invasive NTS in immunocompromised hosts. An increase in multi-drug resistant (MDR) STM strains has been a major concern in the healthcare system and a search for alternative treatments has become imperative. Several probiotic strains have been extensively studied for their role against Salmonella. The Gram-positive bacterium Limosilactobacillus (Lactobacillus) reuteri KUB-AC5 (AC5) isolated from chicken gut has demonstrated an antagonistic effect to STM. However, the differences in STM strains could result in different outcomes of the AC5 intervention. In this study, we investigated the growth inhibitory effect of AC5 on five randomly selected MDR clinical STM strains (STMC) isolated from acute NTS patients admitted to Maharaj Nakorn Chiang Mai Hospital. All five STMCs (SMTC53, 78, 81, 101, and 107) exhibited MDR phenotypes. By using agar spot, cell-free supernatant diffusion agar and liquid medium co-culture assay, we found that AC5 can significantly inhibit the growth of all STMCs. Our study suggested that AC5 has the potential to be a probiotic intervention against STM infection in Thailand.
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References
Gunell M, Aulu L, Jalava J, Lukinmaa-Åberg S, Osterblad M, Ollgren J, et al. Cefotaxime-resistant Salmonella enterica in travelers returning from Thailand to Finland. Emerg Infect Dis. 2014;20(7): 1214-1217.
Whistler T, Sapchookul P, McCormick DW, Sangwichian O, Jorakate P, Makprasert S, et al. Epidemiology and antimicrobial resistance of invasive non-typhoidal Salmonellosis in rural Thailand from 2006-2014. PLoS Negl Trop Dis. 2018;12(8):e0006718.
Kankwatira AM, Mwafulirwa GA, Gordon MA. Non-typhoidal Salmonella bacteraemia--an under-recognized feature of AIDS in African adults. Trop Doct. 2004;34(4):198-200.
Gordon MA, Banda HT, Gondwe M, Gordon SB, Boeree MJ, Walsh AL, et al. Non-typhoidal Salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. AIDS. 2002;16(12):1633-1641.
Carvalho JP, Benusic M, Codat R, Gruescu R, Haydu L, Loh LC. Health risks of frozen raw breaded chicken products: a local health unit perspective. Can Commun Dis Rep. 2020;46(1112):403-408.
Lee H, Yoon Y. Etiological agents implicated in foodborne illness world wide. Food Sci Anim Resour. 2021;41(1):1-7.
Elnekave E, Hong SL, Lim S, Boxrud D, Rovira A, Mather AE, et al. Transmission of multidrug-resistant Salmonella enterica Subspecies enterica 4,[5],12:i:- Sequence Type 34 between Europe and the United States. Emerg Infect Dis. 2020;26(12):3034-3038.
Mather AE, Phuong TLT, Gao Y, Clare S, Mukhopadhyay S, Goulding DA, et al. New variant of multidrug-resistant Salmonella enterica Serovar Typhimurium associated with invasive disease in immunocompromised patients in Vietnam. mBio. 2018;9(5):e01056-18.
Neveling DP, Dicks LMT. Probiotics: an antibiotic replacement strategy for healthy broilers and productive rearing. Probiotics Antimicrob Proteins. 2021;13(1):1-11.
Behnsen J, Deriu E, Sassone-Corsi M, Raffatellu M. Probiotics: properties, examples, and specific applications. Cold Spring Harb Perspect Med. 2013;3(3):a010074.
Shi S, Qi Z, Sheng T, Tu J, Shao Y, Qi K. Antagonistic trait of Lactobacillus reuteri S5 against Salmonella enteritidis and assessment of its potential probiotic characteristics. Microb Pathog. 2019;137:103773.
Nii T, Kakuya H, Isobe N, Yoshimura Y. Lactobacillus reuteri enhances the mucosal barrier function against heat-killed Salmonella Typhimurium in the Intestine of broiler chicks. J Poult Sci. 2020;57(2): 148-59.
Lin CF, Lin MY, Lin CN, Chiou MT, Chen JW, Yang KC, et al. Potential probiotic of Lactobacillus strains isolated from the intestinal tracts of pigs and feces of dogs with antibacterial activity against multidrug-resistant pathogenic bacteria. Arch Microbiol. 2020;202(7):1849-1860.
Jiang P, Yang W, Jin Y, Huang H, Shi C, Jiang Y, et al. Lactobacillus reuteri protects mice against Salmonella typhimurium challenge by activating macrophages to produce nitric oxide. Microb Pathog. 2019;137:103754.
van Zyl WF, Deane SM, Dicks LMT. Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria. Gut Microbes. 2020;12(1):1831339.
Sassone-Corsi M, Raffatellu M. No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J Immunol. 2015;194(9):4081-4087.
Heredia-Castro PY, Reyes-Diaz R, Rendon-Rosales MA, Beltran-Barrientos LM, Torres-Llanez MJ, Estrada-Montoya MC, et al. Novel bacteriocins produced by Lactobacillus fermentum strains with bacteriostatic effects in milk against selected indicator microorganisms. J Dairy Sci. 2021;S0022-0302(21):00170-3.
Meng J, Wang YY, Hao YP. Protective function of surface layer protein from Lactobacillus casei fb05 against intestinal pathogens in vitro. Biochem Biophys Res Commun. 2021;546:15-20.
McCormick TS, Weinberg A. Epithelial cell-derived antimicrobial peptides are multifunctional agents that bridge innate and adaptive immunity. Periodontol 2000. 2010;54(1):195-206.
Mantis NJ, Rol N, Corthesy B. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 2011;4(6):603-611.
Nitisinprasert S, Nilphai V, Bunyun P, Sukyai P, Doi K, Sonomoto K. Screening and identification of effective thermotolerant lactic acid bacteria producing antimicrobial activity against Escherichia coli and Salmonella sp. resistant to antibiotics. Agriculture and Natural Resources. 2000;34(3):387-400.
Nakphaichit M, Thanomwongwattana S, Phraephaisarn C, Sakamoto N, Keawsompong S, Nakayama J, et al. The effect of including Lactobacillus reuteri KUB-AC5 during post-hatch feeding on the growth and ileum microbiota of broiler chickens. Poult Sci. 2011;90(12):2753-2765.
Nakphaichit M, Sobanbua S, Siemuang S, Vongsangnak W, Nakayama J, Nitisinprasert S. Protective effect of Lactobacillus reuteri KUB-AC5 against Salmonella enteritidis challenge in chickens. Benef Microbes. 2019;10(1):43-54.
Baumler AJ, Winter SE, Thiennimitr P, Casadesus J. Intestinal and chronic infections: Salmonella lifestyles in hostile environments. Environ Microbiol Rep. 2011;3(5):508-517.
Branchu P, Bawn M, Kingsley RA. Genome variation and molecular epidemiology of Salmonella enterica Serovar typhimurium pathovariants. Infect Immun. 2018;86(8).
Sarichai P, Buddhasiri S, Walters GE, Khantawa B, Kaewsakhorn T, Chantarasakha K, et al. Pathogenicity of clinical Salmonella enterica serovar typhimurium isolates from Thailand in a mouse colitis model. Microbiol Immunol. 2020;64(10):679-693.
CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 28th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2018.
Jacobsen CN, Rosenfeldt Nielsen V, Hayford AE, Moller PL, Michaelsen KF, Paerregaard A, et al. Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol. 1999;65(11):4949-49456.
Drago L, Gismondo MR, Lombardi A, de Haen C, Gozzini L. Inhibition of in vitro growth of enteropathogens by new Lactobacillus isolates of human intestinal origin. FEMS Microbiol Lett. 1997;153(2):455-463.
Chen C, Li J, Zhang H, Xie Y, Xiong L, Liu H, et al. Effects of a probiotic on the growth performance, intestinal flora, and immune function of chicks infected with Salmonella pullorum. Poult Sci. 2020;99(11):5316-5323.
Adetoye A, Pinloche E, Adeniyi BA, Ayeni FA. Characterization and anti-salmonella activities of lactic acid bacteria isolated from cattle faeces. BMC Microbiology. 2018;18(1):96.
Lima ET, Andreatti Filho RL, Okamoto AS, Noujaim JC, Barros MR, Crocci AJ. Evaluation in vitro of the antagonistic substances produced by Lactobacillus spp. isolated from chickens. Can J Vet Res. 2007;71(2):103-107.
Sobanbua S, Tangthong J, Suveatwatanakul A, Nakphaichit M, Keawsompong S, Nitisinprasert S. Cloning and expression of the antimicrobial peptide from Lactobacillus reuteri KUB-AC5 and its characterization. IJAT. 2020:1013-36.
Buddhasiri S, Sukjoi C, Kaewsakhorn T, Nambunmee K, Nakphaichit M, Nitisinprasert S, et al. Anti-inflammatory effect of probiotic Limosilactobacillus reuteri KUB-AC5 against Salmonella infection in a mouse colitis model. Front Microbiol. 2021;12:716761.
Drago L, Gismondo MR, Lombardi A, de Haën C, Gozzini L. Inhibition of in vitro growth of enteropathogens by new Lactobacillus isolates of human intestinal origin. FEMS Microbiology Letters. 1997;153(2):455-463.