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.李斯特菌属（Listeria）具有异质性，包含致病性与非致病性菌种。致病性单核细胞增生李斯特菌（L. monocytogenes）与伊万诺夫李斯特菌（L. ivanovii）具有不同的环境分布特征，感染不同宿主，并引发特征各异的临床综合征。本研究旨在评估不同李斯特菌种对多样宿主微环境的应答，是否会影响其毒力异质性并改变其环境分布。我们检测了受试菌种对胃液、肠液、肠道及子宫微生物群与精液的抗性。结果显示：单核细胞增生李斯特菌在胃液中的抗性显著强于伊万诺夫李斯特菌，而塞利格李斯特菌（L. seeligeri）与瓦伦蒂娜李斯特菌（L. valentina）则表现出中间型抗性表型；所有受试李斯特菌种均可耐受肠液。肠道微生物群可竞争性抑制并清除伊万诺夫李斯特菌与瓦伦蒂娜李斯特菌，但单核细胞增生李斯特菌与塞利格李斯特菌可竞争性抑制肠道共生菌。本研究结果表明，与单核细胞增生李斯特菌和塞利格李斯特菌不同，受试伊万诺夫李斯特菌难以在反刍动物胃肠道内定殖，这将减少其复制、粪便排毒与环境扩散。然而，伊万诺夫李斯特菌可在子宫微生物群与精液中存活的能力提示，受试菌株可在反刍动物的泌尿生殖道中长期存留。因此，性传播途径相较于经口传播更为可行，这或可解释为何伊万诺夫李斯特菌与流产暴发相关，而非脑炎病例。