Multifaceted Defense against Listeria monocytogenes in the Gastro-Intestinal Lumen

Abstract

Listeria monocytogenes is a foodborne pathogen that can cause febrile gastroenteritis in healthy subjects and systemic infections in immunocompromised individuals. Despite the high prevalence of L. monocytogenes in the environment and frequent contamination of uncooked meat and poultry products, infections with this pathogen are relatively uncommon, suggesting that protective defenses in the general population are effective. In the mammalian gastrointestinal tract, a variety of defense mechanisms prevent L. monocytogenes growth, epithelial penetration and systemic dissemination. Among these defenses, colonization resistance mediated by the gut microbiota is crucial in protection against a range of intestinal pathogens, including L. monocytogenes. Here we review defined mechanisms of defense against L. monocytogenes in the lumen of the gastro-intestinal tract, with particular emphasis on protection conferred by the autochthonous microbiota. We suggest that selected probiotic species derived from the microbiota may be developed for eventual clinical use to enhance resistance against L. monocytogenes infections.

Enhancing mucosal immunity by transient microbiota depletion

“…Given the immunogenic effects produced by LmOVA expansion in the gut lumen, we hypothesized that maintaining or restoring high densities of this vector over time might further increase expansion of CD8 + Trm cells. As microbiota-mediated colonization resistance represents the main mechanism by which Lm density is reduced in the gut lumen 21 , we reasoned that repeated administration of streptomycin, to which Lm is resistant, could serve this purpose by impairing recovery of commensal microbes. As predicted, streptomycin gavage at day −1, 4, and 9 with respect to Lm inoculum, resulted in sustained, high-density fecal shedding of LmOVA and induced dramatic accumulation of antigen-specific CD8 + T cells in the LILP, which at day 45-70 post immunization were~100-fold more abundant than those detected in mice administered standard immunization (Fig.…”

Ecogenetics of antibiotic resistance in Listeria monocytogenes

“…There are probably strain-specific impediments preventing successful transmission of resistance plasmids (Anisimova & Yarullina, 2018). Interestingly, most of these genera produce bacteriocins that inhibit the growth of L. monocytogenes (Arihara, Cassens, & Luchansky, 1993;Becattini et al, 2017;Becattini & Pamer, 2018;Fisher & Phillips, 2009), possibly impairing cell-to-cell contact. L. monocytogenes lineage II, which is more resistant to bacteriocins, harbors plasmids more often than lineage I (Orsi, Bakker, & Wiedmann, 2011).…”

Food-Associated Stress Primes Foodborne Pathogens for the Gastrointestinal Phase of Infection

“…Saliva in the mouth contains bacteriolytic enzymes (lysozyme), and gastric juice in the stomach contains hydrochloric acid and digestive enzymes, while the small and large intestine contain antimicrobial peptides (defensins, cathelicidin, cryptdin, elafin, etc. ), bile, natural microflora, mucus, secretory IgA, oxygen-limiting environment, epithelial barrier, and submucosal immune cells ( Brogden, 2005 ; Wesche et al, 2009 ; Garrett et al, 2010 ; Jäger et al, 2010 ; Sleator and Hill, 2010 ; Becattini and Pamer, 2017 ; Bhunia, 2018 ). Pathogens encounter multiple host-induced stresses in the intestine from acidic pH, nutrient limitation, low iron, oxidative and nitrosative stress, bile salts, free fatty acids, DNA damage, oxygen-limitation, and temperature in the gut ( Louis and O’Byrne, 2010 ; Fang et al, 2016 ).…”

“…Lipocalin-2 production is stimulated by the host inflammatory response and binds siderophores, thus limiting iron uptake and preventing microbial growth ( Flo et al, 2004 ; Raffatellu et al, 2009 ). Commensal microbes can protect the host from pathogenic microbes through competitive exclusion and production of antimicrobial peptides (bacteriocins) although some pathogenic microbes can evade such a barrier ( Cotter et al, 2005a ; Hibbing et al, 2010 ; Becattini and Pamer, 2017 ).…”