Factors contributing to Listeria monocytogenes transmission and impact on food safety
Graphical abstract
Introduction
Listeria monocytogenes (Lm) is one of the most significant foodborne pathogens in the European Union [1]. Understanding its biology is an active field of research. From 2017 to 2020, almost 2000 papers referring to ‘Listeria’ in their titles have been referenced in Web of Science. After decades of work, Lm has become a model of infection biology [2,3], but other facets of its lifestyle remain to be elucidated. One intriguing aspect is the variety of habitats where it can be found (Figure 1). From outdoor environments to food companies, and occasionally animal hosts, the routes of transmission are complex. Lm encounters a large array of environmental conditions during these transfers from one habitat to the other and physiological adaptation to the surroundings is a prerequisite for its persistence. A recent H2020 MSCA European Training Network (List_MAPS) focused on the intrinsic and extrinsic factors contributing to the ubiquity of Lm and its persistence in several habitats (natural outdoor environments, biofilms, food, the intestinal tract). This review focuses on the most recent advances in this field according to the literature published from 2017 to April 2020, including the major outcomes of List_MAPS (https://cordis.europa.eu/project/id/641984).
Section snippets
Outdoor environments as a reservoir of Lm and pre-harvest routes of transmission
From a food safety point of view, outdoor environments can be considered as a reservoir of Lm. Continuous reporting of the detection of Listeria spp. and Lm in soil confirms that it is a habitat of the pathogenic species. A survey in wild Colorado documented pristine ecosystems as reservoirs of members of Listeria spp. and Lm although the incidence was low [4]. Another study from Northern America reported a high incidence of Lm in wild bears, confirming wildlife as reservoir of virulent and
Regulation: regulators, sigma factors and sRNAs
Transmission from one habitat to the other relies on the ability of a bacterium to cope with the new environmental conditions and to adjust its physiology to the characteristics of the new habitat. Regulation is central in this process. Lm avails of a large array of regulatory proteins and small regulatory RNAs (sRNAs). Among sigma factors, Sigma B has a major role in stress response and virulence as detailed in recent reviews [36,37]. Moreover, Sigma B activity is required in outdoor
Metabolism and impact of carbon source
Energy production is essential for the persistence of any organism in a habitat. Lm avails of a large array of transporters and catabolic pathways that enable utilisation of diverse resources according to the conditions of the habitat. As such, metabolism is the cornerstone of habitat colonisation. Information on the metabolic processes of Lm can be found in recent reviews [49,50].
As a facultative anaerobic organism, the metabolism of Lm depends on the presence or absence of oxygen. For
Role of diet and the microbiota in Lm infection
Diet and the microbiota have emerged as major factors influencing local (gastrointestinal) and systemic immunity, gut barrier function and susceptibility to infectious disease. Dietary components have direct modulatory effects upon cells of the immune system [58], influence gut microbiota composition [58] and production of bacterial signalling compounds (short-chain fatty acids, lipopolysaccharide and bile acids) [59] and may directly influence the pathogen through regulation of virulence gene
Diversity and phenotypic characteristics
Among the factors contributing to the transmission of Lm, intraspecific factors play obviously a major role. Whole Genome Sequencing (WGS) paved the way for in-depth investigation of the intraspecific diversity and population biology of Lm. The pioneering work by Moura et al. inferred the population structure of Lm from a collection of 1696 isolates from diverse food, clinical and geographical origins [73••]. The genome of Lm is highly stable. Four lineages are identified and most isolates are
Conclusion
Lm is a versatile bacterium found in many habitats. Among the routes leading to contamination of food, its transmission depends on a combination of extrinsic (environmental characteristics) and intrinsic factors (intraspecific diversity, metabolism, regulatory circuitry). Food safety requires constant surveillance. Proper environmental monitoring in food processing facilities is needed to control contamination [92] and WGS is becoming the standard for epidemiology, surveillance [73••,93] and
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
BKM, CGMG and PP acknowledge funding from the European Union in the form of a Marie Curie ITN grant (H2020-MSCA-ITN-2014-ETN LIST_MAPS, Grant Agreement n°: 641984). CGMG acknowledges funding and support from Science Foundation Ireland (SFI) in the form of a center grant (APC Microbiome Ireland grant SFI/12/RC/2273).
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These two authors participated equally to the review.