Department of Food and Nutrition, Chungbuk National University, Chengju, Chungbuk, South Korea.
Department of Food, Bioprocessing and Nutrition Sciences, North Carolina State University, Raleigh, North Carolina, USA.
Appl Environ Microbiol. 2023 Feb 28;89(2):e0209722. doi: 10.1128/aem.02097-22. Epub 2023 Feb 2.
Listeria monocytogenes causes the severe foodborne disease listeriosis. Several clonal groups of L. monocytogenes possess the pathogenicity islands pathogenicity island 3 (LIPI-3) and LIPI-4. Here, we investigated the prevalence and genetic diversity of LIPI-3 and LIPI-4 among 63 strains of seven nonpathogenic spp. from the natural environment, i.e., wildlife (black bears []) and surface water. Analysis of the whole-genome sequence data suggested that both islands were horizontally acquired but differed considerably in their incidence and genetic diversity. LIPI-3 was identified among half of the strains in the same genomic location as in L. monocytogenes ( hot spot) in a truncated form, with only three strains harboring full-length LIPI-3, and a highly divergent partial LIPI-3 was observed in three Listeria seeligeri strains, outside the hot spot. Premature stop codons (PMSCs) and frameshifts were frequently noted in the LIPI-3 gene encoding listeriolysin S. On the other hand, full-length LIPI-4 without any PMSCs was found in all Listeria innocua strains, in the same genomic location as L. monocytogenes and with ~85% similarity to the L. monocytogenes counterpart. Our study provides intriguing examples of genetic changes that pathogenicity islands may undergo in nonpathogenic bacterial species, potentially in response to environmental pressures that promote either maintenance or degeneration of the islands. Investigations of the roles that LIPI-3 and LIPI-4 play in nonpathogenic spp. are warranted to further understand the differential evolution of genetic elements in pathogenic versus nonpathogenic hosts of the same genus. Listeria monocytogenes is a serious foodborne pathogen that can harbor the pathogenicity islands pathogenicity island 3 (LIPI-3) and LIPI-4. Intriguingly, these have also been reported in nonpathogenic from food and farm environments, though limited information is available for strains from the natural environment. Here, we analyzed whole-genome sequence data of nonpathogenic spp. from wildlife and surface water to further elucidate the genetic diversity and evolution of LIPI-3 and LIPI-4 in . While the full-length islands were found only in , LIPI-3 was uncommon and exhibited frequent truncation and genetic diversification, while LIPI-4 was remarkable in being ubiquitous, albeit diversified from L. monocytogenes. These contrasting features demonstrate that pathogenicity islands in nonpathogenic hosts can evolve along different trajectories, leading to either degeneration or maintenance, and highlight the need to examine their physiological roles in nonpathogenic hosts.
李斯特菌属引起严重的食源性疾病李斯特菌病。几个李斯特菌属的克隆群拥有致病性岛 3 (LIPI-3) 和 LIPI-4。在这里，我们研究了来自自然环境的 7 种非致病性 种的 63 株菌中 LIPI-3 和 LIPI-4 的流行情况和遗传多样性，包括野生动物（黑熊 []) 和地表水。全基因组序列数据分析表明，这两个岛都是水平获得的，但在发病率和遗传多样性上有很大的差异。LIPI-3 被鉴定为一半的 菌株位于与李斯特菌属相同的基因组位置（热点），呈截断形式，只有 3 株菌含有全长 LIPI-3，而 3 株李斯特菌属 seeligeri 菌株中的 LIPI-3 高度分化，位于 热点之外。在编码李斯特菌溶素 S 的 LIPI-3 基因中经常发现提前终止密码子（PMSCs）和移码。另一方面，所有 Listeria innocua 株都发现了全长 LIPI-4，没有任何 PMSCs，位于与李斯特菌属相同的基因组位置，与李斯特菌属的对应物有~85%的相似性。我们的研究提供了有趣的例子，说明致病性岛在非致病性细菌物种中可能发生的遗传变化，这可能是对促进岛屿维持或退化的环境压力的反应。调查 LIPI-3 和 LIPI-4 在非致病性 中的作用，有助于进一步了解同一属中致病性和非致病性宿主遗传元素的差异进化。李斯特菌属是一种严重的食源性病原体，可携带致病性岛 3 (LIPI-3) 和 LIPI-4。有趣的是，这些岛也在食品和农场环境中的非致病性 中被报道过，尽管关于来自自然环境的菌株的信息有限。在这里，我们分析了来自野生动物和地表水的非致病性 种的全基因组序列数据，以进一步阐明 LIPI-3 和 LIPI-4 在 中的遗传多样性和进化。虽然全长岛只在 中发现，但 LIPI-3 并不常见，经常发生截断和遗传多样化，而 LIPI-4 则非常普遍，尽管与李斯特菌属不同。这些对比特征表明，非致病性宿主中的致病性岛可以沿着不同的轨迹进化，导致退化或维持，并强调需要在非致病性宿主中检查它们的生理作用。
