Listeria monocytogenes is a saprophytic gram-positive bacterium, and an opportunistic foodborne pathogen that can produce listeriosis in humans and animals. It has evolved an exceptional ability to adapt to stress conditions encountered in different environments, resulting in a ubiquitous distribution. Because some food preservation methods and disinfection protocols in food-processing environments cannot efficiently prevent contaminations, L. monocytogenes constitutes a threat to human health and a challenge to food safety. In the host, Listeria colonizes the gastrointestinal tract, crosses the intestinal barrier, and disseminates through the blood to target organs. In immunocompromised individuals, the elderly, and pregnant women, the pathogen can cross the blood-brain and placental barriers, leading to neurolisteriosis and materno-fetal listeriosis. Molecular and cell biology studies of infection have proven L. monocytogenes to be a versatile pathogen that deploys unique strategies to invade different cell types, survive and move inside the eukaryotic host cell, and spread from cell to cell. Here, we present the multifaceted Listeria life cycle from a comprehensive perspective. We discuss genetic features of pathogenic Listeria species, analyze factors involved in food contamination, and review bacterial strategies to tolerate stresses encountered both during food processing and along the host’s gastrointestinal tract. Then we dissect host–pathogen interactions underlying listerial pathogenesis in mammals from a cell biology and systemic point of view. Finally, we summarize the epidemiology, pathophysiology, and clinical features of listeriosis in humans and animals. This work aims to gather information from different fields crucial for a comprehensive understanding of the pathogenesis of L. monocytogenes.

Listeria monocytogenes (Lm) is a major human and animal foodborne pathogen. However, data from environmental reservoirs remain scarce. Here, we used whole genome sequencing to characterize Listeria spp. isolates recovered over one year from wild animals in their natural habitats in Spain. Three different Listeria spp. [Lm (n=19), Listeria ivanovii subsp. londoniensis (Liv, n=4) and Listeria innocua (Lin, n=3)] were detected in 23 animal tonsils (9 deer, 14 wild boars) and 2 feeding throughs. No Listeria spp. was detected in feces. Lm was detected in tonsils of 44.4% (8 out of 18) deer and 40.7% (11 out of 27) wild boars. Lm isolates belonged to 3 different cgMLST types (CTs) of 3 distinct sublineages (SL1, SL387 and SL155) from lineages I and II. While cgMLST type L1-SL1-ST1-CT5279 (IVb, CC1) occurred only in one animal, types L1-SL387-ST388-CT5239 (IVb, CC388) and L2-SL155-ST155-CT1170 (IIa, CC155) were retrieved from multiple animals. In addition, L1-SL387-ST388-CT5239 (IVb, CC388) isolates were collected 1 year apart, revealing its long-term occurrence within the animal population and/or environmental reservoir. The presence of identical Lm strains in deer and wild boars suggest contamination from a common food or environmental source, although interhost transmission cannot be excluded. Pathogenicity islands were present in 100% (LIPI-1), 5% (LIPI-3) and 79% (LIPI-4) of the Lm isolates and all Lm lineage II isolates (n=3) carried SSI-1 stress islands. This study highlights the need for monitoring Lm environmental contamination and the importance of tonsils as a possible Lm intra-host reservoir. Importance: Listeria monocytogenes (Lm) is a foodborne bacterial pathogen responsible for listeriosis. Whole genome sequencing has been extensively used in public health and food industries to characterize circulating Listeria isolates, but genomic data on isolates occurring in natural environments and wild animals is still scarce. Here, we show that wild animals carry pathogenic Listeria and that the same genotypes can be found at different time points in different host species. This work highlights the need of Listeria spp. monitoring of environmental contamination and the importance of tonsils as a possible Lm intra-host reservoir.

Studies have shown that ruminants constitute reservoirs of Listeria monocytogenes, but little is known about the epidemiology and genetic diversity of this pathogen within farms. Here we conducted a largescale longitudinal study to monitor Listeria spp. in 19 dairy farms during three consecutive seasons (N = 3251 samples). L. innocua was the most prevalent species, followed by L. monocytogenes. Listeria monocytogenes was detected in 52.6% of farms and more frequently in cattle (4.1%) and sheep (4.5%) than in goat farms (0.2%). Lineage I accounted for 69% of L. monocytogenes isolates. Among animal samples, the most prevalent sublineages (SL) and clonal complexes (CC) were SL1/CC1, SL219/CC4, SL26/CC26 and SL87/CC87, whereas SL666/CC666 was most prevalent in environmental samples. Sixtyone different L. monocytogenes cgMLST types were found, 28% common to different animals and/or surfaces within the same farm and 21% previously reported elsewhere in the context of food and human surveillance. Listeria monocytogenes prevalence was not affected by farm hygiene but by season: higher prevalence was observed during winter in cattle, and during winter and spring in sheep farms. Cows in their second lactation had a higher probability of L. monocytogenes faecal shedding. This study highlights dairy farms as a reservoir for hypervirulent L. monocytogenes.

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The increasing prevalence of Listeria monocytogenes infections is a public health issue. Although studies have shown that ruminants constitute reservoirs of this foodborne pathogen, little is known about its epidemiology and genetic diversity within ruminant farms. Here we conducted a large-scale genomic and epidemiologic longitudinal study of Listeria spp. in dairy ruminants and their environments, comprising 19 farms monitored for three consecutive seasons (N=3251 samples). L. innocua was the most prevalent Listeria spp, followed by L. monocytogenes. L. monocytogenes was detected in 52.6% of farms (prevalence in feces samples 3.8%, in farm environment samples 2.5%) and more frequently in cattle (4.1%) and sheep (4.5%) than in goat farms (0.2%). Lineage I accounted for 69% of L. monocytogenes isolates. Among animal samples, the most prevalent sublineages (SL) and clonal complexes (CC) were SL1/CC1, SL219/CC4, SL26/CC26 and SL87/CC87, whereas SL666/CC666 was prevalent in environmental samples. 61 different L. monocytogenes CTs (cgMLST sequence types) were found, 17 of them (27.9%) common to different animals and/or surfaces within the same farms. L. monocytogenes prevalence was not affected by farm hygiene but by season: the overall prevalence of L. monocytogenes in cattle farms was higher during winter, and in sheep farms was higher during winter and spring. Cows in their second lactation had a higher probability of L. monocytogenes fecal shedding than other lactating cows. This study highlights that dairy farms constitute a reservoir for hypervirulent L. monocytogenes and the importance of continuous animal surveillance to reduce the burden of human listeriosis.