Contrasting genetic diversity of Listeria pathogenicity islands 3 and 4 harbored by non-pathogenic Listeria spp

Authors: LEE, SANGMI - Chungbuk National University; PARSONS, CAMERON - North Carolina State University; CHEN, YI - Food And Drug Administration(FDA); Dungan, Robert - Rob; KATHARIOU, SOPHIA - North Carolina State University

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/6/2023
Publication Date: 2/2/2023
Citation: Lee, S., Parsons, C., Chen, Y., Dungan, R.S., Kathariou, S. 2023. Contrasting genetic diversity of Listeria pathogenicity islands 3 and 4 harbored by non-pathogenic Listeria spp. Applied and Environmental Microbiology. 89(2). Article e02097-22. https://doi.org/10.1128/aem.02097-22.
DOI: https://doi.org/10.1128/aem.02097-22

Interpretive Summary: The bacterium, Listeria monocytogenes, causes the severe foodborne disease listeriosis and its capacity to do so is related to the presence of genomic or pathogenicity islands. In this study, we investigated the prevalence and genetic diversity of pathogenicity islands among 63 strains of seven non-pathogenic Listeria species from the natural environment. Analysis of whole genome sequence data indicated that two different pathogenicity islands (LIPI-3 and LIPI-4) were horizontally acquired, but each differed considerably in their incidence and genetic diversity. Horizontal gene transfer is the transfer of genes between bacteria, which can occur via three different mechanisms. Interestingly, full-length pathogenicity islands were found in non-pathogenic Listeria innocua strains, which occurs in the same genomic location as Listeria monocytogenes. Pathogenicity islands are usually absent from non-pathogenic organisms of the same or closely related species. This study provides examples of genetic changes that pathogenicity islands my undergo in non-pathogenic Listeria in response to environmental pressures that either promote island maintenance or degeneration. Further investigations into the role of pathogenicity islands in non-pathogenic Listeria species are warranted to better understand the evolution of genetic elements in pathogenic versus non-pathogenic hosts of the same genus.

Technical Abstract: Listeria monocytogenes causes the severe foodborne disease listeriosis. Several clonal groups of L. monocytogenes possess the pathogenicity islands Listeria 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 non-pathogenic Listeria species from the natural environment (i.e., wildlife and surface waters). 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 Listeria innocua strains in the same genomic location as Listeria monocytogenes (guaA hotspot) 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 guaA hotspot. 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 non-pathogenic 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 non-pathogenic Listeria species are warranted to further understand the differential evolution of genetic elements in pathogenic versus non-pathogenic hosts of the same genus.