Tissue-specific microbiota dictates the competitive dynamics of <i>Listeria</i> species colonization

The genus <i>Listeria</i> is heterogeneous and contains pathogenic and nonpathogenic species. Pathogenic <i>L. monocytogenes</i> and <i>L. ivanovii</i> have different environmental distributions, infect different hosts, and cause distinct syndromes. Here, we evaluated whether responses of different <i>Listeria</i> 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. <i>L. monocytogenes</i> was more resistant than <i>L. ivanovii</i> in gastric fluid, whilst <i>L. seeligeri</i> and <i>L. valentina</i> showed an intermediate phenotype. All the tested <i>Listeria</i> species resisted the intestinal fluid. Gut microbial communities outcompeted and eliminated <i>L. ivanovii</i> and <i>L. valentina</i>. However, <i>L. monocytogenes</i> and <i>L. seeligeri</i> outcompeted intestinal commensal bacteria. Our findings suggest that, unlike <i>L. monocytogenes</i> and <i>L. seeligeri</i>, the tested <i>L. ivanovii</i> are unlikely to colonize the gastrointestinal tract of ruminants, which would reduce replication, fecal shedding, and environmental distribution. However, the ability of <i>L. ivanovii</i> 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 <i>L. ivanovii</i> is associated with abortion outbreaks and not encephalitic cases.