The interaction between Listeria monocytogenes and the host gastrointestinal tract

Abstract

Listeria monocytogenes is a ubiquitous bacterium that causes significant foodborne disease with high mortality rates in immunocompromised adults. In pregnant women foodborne infection can give rise to infection of the fetus resulting in miscarriage. In addition, the bacterium has recently been demonstrated to cause localized gastrointestinal symptoms, predominantly in immunocompetent individuals. The murine model of systemic L. monocytogenes infection has provided numerous insights into the mechanisms of pathogenesis of this organism. However, recent application of transcriptomic and proteomic approaches as well as the development of new model systems has allowed a focus upon factors that influence adaptation to gastrointestinal environments and adhesion to and invasion of the gastrointestinal mucosa. In addition, the availability of a large number of complete L. monocytogenes genome sequences has permitted inter-strain comparisons and the identification of factors that may influence the emergence of 'epidemic' phenotypes. Here we review some of the exciting recent developments in the analysis of the interaction between L. monocytogenes and the host gastrointestinal tract. IntroductionListeria monocytogenes is a Gram-positive foodborne pathogen that is the causative agent of listeriosis, a disease which manifests primarily as meningitis or meningoencephalitis in non-pregnant individuals, or as infection of the fetus in pregnant women. L. monocytogenes normally resides in decaying plant matter in the soil but may be transiently associated with the gastrointestinal (GI) tract in a number of animal species. The pathogen may also cause systemic disease in domestic animals, including sheep and cattle, leading to circling disease in adult animals or spontaneous abortion in pregnant animals (Czuprynski, 2005). Infection by, or indeed carriage of the pathogen by domestic animals poses a risk of zoonotic transmission through contaminated milk or meat. Contaminated raw foodstuffs that are subjected to minimal further processing are likely to pose the greatest risk to human health; such foodstuffs include soft cheeses, pâtés, frankfurters and post-process contaminated milk (Swaminathan & GernerSmidt, 2007).Clearly L. monocytogenes encounters the mammalian GI tract at a number of stages during the infectious cycle: potentially during asymptomatic intestinal carriage or prior to causation of animal disease and then during infection of the human host before invasion of the GI epithelium. The genome of the bacterium reflects this ability to adapt to a variety of environments, containing a complex arsenal of genes encoding regulatory proteins as well as genes encoding proteins linked to survival within the GI tract, including bile salt hydrolase (bsh) and bile exclusion protein (bilE) (Begley et al., 2005;Dussurget et al., 2002;Glaser et al., 2001;Sleator et al., 2005).We and others have previously described the physiological adaptation of L. monocytogenes during passage from external environments to the host GI tract Gray et a...

LysPGS formation inListeria monocytogeneshas broad roles in maintaining membrane integrity beyond antimicrobial peptide resistance

“…5 The involvement of L. monocytogenes-encoded internalin proteins and listeriolysin-O in this intracellular invasion process are well documented. 6 It is likely that additional mechanisms for evasion of the host immune system remain unidentified or under-characterized in the case of this bacterium including, for example, lipid aminoacylation. 7 In many pathogens, changes occur in the composition of the lipid bilayer in response to various environmental stressors including those specifically encountered upon infection of the host.…”

Lmo0036, an ornithine and putrescine carbamoyltransferase in Listeria monocytogenes, participates in arginine deiminase and agmatine deiminase pathways and mediates acid tolerance

“…An elevated level of acid is often added to foods to inhibit bacterial growth (Byelashov et al, 2010). After ingestion via contaminated foods, L. monocytogenes encounters the acidic conditions of the gastric barrier, followed by exposure to fatty acid in the intestine (Sleator et al, 2009). Survival in the host gastrointestinal tract is the key stage for initiating listerial infection.…”

“…Among the four evolutionary lineages, only lineages I and II are commonly isolated from contaminated foods and human listeriosis patients (Orsi et al, 2011;Ward et al, 2008). The virulence potential of L. monocytogenes is linked to its ability to survive adverse environmental conditions encountered both in natural environments and subsequently within the host (Ryan et al, 2009;Sleator et al, 2009). An elevated level of acid is often added to foods to inhibit bacterial growth (Byelashov et al, 2010).…”

Proteins

“…In prokaryote genomes the loci of functionally related proteins tend to be co-located on the chromosome; an example of this are the membrane bound ABC transport proteins OpuC and OpuB(BilE) of Listeria monocytogenes which are separated by only 2.4 Kb 39 on the listerial chromosome and contribute to bile resistance in this gastrointestinal pathogen. [40][41][42][43] As an extension of chromosomal proximity, genes involved in similar cellular functions also tend to be co-transcribed as has also been shown to be the case with opuC and opuB(bilE).…”