Tissue-specific microbiota dictates the competitive dynamics of Listeria species colonization

The genus Listeria is heterogeneous and contains pathogenic and nonpathogenic species. Pathogenic L. monocytogenes and L. ivanovii have different environmental distributions, infect different hosts, and cause distinct syndromes. Here, we evaluated whether responses of different Listeria species to diverse host niches contribute to virulence heterogeneity and influence their environmental distribution. We assessed resistance to gastric and intestinal fluids, gut and uterus microbiota, and semen. L. monocytogenes was more resistant than L. ivanovii in gastric fluid, whilst L. seeligeri and L. valentina showed an intermediate phenotype. All the tested Listeria species resisted the intestinal fluid. Gut microbial communities outcompeted and eliminated L. ivanovii and L. valentina. However, L. monocytogenes and L. seeligeri outcompeted intestinal commensal bacteria. Our findings suggest that, unlike L. monocytogenes and L. seeligeri, the tested L. ivanovii are unlikely to colonize the gastrointestinal tract of ruminants, which would reduce replication, fecal shedding, and environmental distribution. However, the ability of L. ivanovii to survive within uterine microbiota and semen suggests that the tested clones could persist in the urogenital tract of ruminants. Then venereal transmission could be more probable than the oral route, which could explain why L. ivanovii is associated with abortion outbreaks and not encephalitic cases.