The Viable But Non-Culturable State of Listeria monocytogenes in the One-Health Continuum

Abstract

Many bacterial species, including several pathogens, can enter a so-called “viable but non-culturable” (VBNC) state when subjected to stress. Bacteria in the VBNC state are metabolically active but have lost their ability to grow on standard culture media, which compromises their detection by conventional techniques based on bacterial division. Under certain conditions, VBNC bacteria can regain their growth capacity and, for pathogens, their virulence potential, through a process called resuscitation. Here, we review the current state of knowledge of the VBNC state of Listeria monocytogenes (Lm), a Gram-positive pathogenic bacterium responsible for listeriosis, one of the most dangerous foodborne zoonosis. After a brief summary of characteristics of VBNC bacteria, we highlight work on VBNC Lm in the environment and in agricultural and food industry settings, with particular emphasis on the impact of antimicrobial treatments. We subsequently discuss recent data suggesting that Lm can enter the VBNC state in the host, raising the possibility that VBNC forms contribute to the asymptomatic carriage of this pathogen in wildlife, livestock and even humans. We also consider the resuscitation and virulence potential of VBNC Lm and the danger posed by these bacteria to at-risk individuals, particularly pregnant women. Overall, we put forth the hypothesis that VBNC forms contribute to adaptation, persistence, and transmission of Lm between different ecological niches in the One-Health continuum, and suggest that screening for healthy carriers, using alternative techniques to culture-based enrichment methods, should better prevent listeriosis risks.

Diving into bacterial dormancy: emergence of osmotically stable wall-less forms in an aquatic environment

“…Some bacteria, mostly Gram-negative species, have been shown to exit the VBNC state and regain culturability under specific “resuscitation” conditions (Ayrapetyan et al, 2018; Dong et al, 2020). Reversion of the VBNC state in Lm and other Gram-positive bacteria remains a challenge (Dong et al, 2020; Lotoux et al, 2022). Revival attempts through nutrient supplementation (e.g.…”

Asymptomatic Carriage of Listeria monocytogenes by Animals and Humans and Its Impact on the Food Chain

“…L. monocytogenes was found in up to 27% of the samples of pond water [ 98 ] and in up to up to 99% in the waste water of stabilization ponds in the arctic region of Canada [ 99 ]. In addition, the ability of L. monocytogenes to enter the VBNC state may contribute to adaptation, persistence and transmission between different ecological niches [ 11 ].…”

“…Truncated forms of the inlA gene were associated with a loss of virulence [ 8 ], which may lead to asymptomatic carriage, and were also overrepresented in isolates from food compared to clinical isolates [ 9 ], suggesting the potential exposure of consumers to these isolates. Additionally, a contribution of viable but nonculturable (VBNC) forms of L. monocytogenes [ 10 ] to asymptomatic carriage has been hypothesized [ 11 , 12 ].…”

Comparative Analysis Using Raman Spectroscopy of the Cellular Constituents of Lacticaseibacillus paracasei Zhang in a Normal and Viable but Nonculturable State

“…Adverse environments, such as radiation, low temperatures, starvation, and antibiotic use, can induce the bacterial VBNC state [ 10 , 11 ]. To date, more than 100 pathogenic and non-pathogenic bacteria have been reported to enter the VBNC state, and most studies on VBNC cells have focused on pathogenic bacteria [ 12 , 13 , 14 ]. Normal cells and VBNC cells exhibit obvious differences in their morphology and physiology, as well as compositional differences in their cell walls, cell membranes, and intramolecular content [ 15 , 16 ].…”