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Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States
Ruminants are a well-known reservoir for Listeria monocytogenes. In addition to asymptomatic carriage of the pathogen, ruminants can also acquire listeriosis and develop clinical manifestations in the form of neurologic or fetal infections, similar to those occurring in humans. Genomic characterizat...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769944/ https://www.ncbi.nlm.nih.gov/pubmed/36314928 http://dx.doi.org/10.1128/spectrum.01579-22 |
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author | Cardenas-Alvarez, Maria X. Zeng, Hui Webb, Brett T. Mani, Rinosh Muñoz, Marina Bergholz, Teresa M. |
author_facet | Cardenas-Alvarez, Maria X. Zeng, Hui Webb, Brett T. Mani, Rinosh Muñoz, Marina Bergholz, Teresa M. |
author_sort | Cardenas-Alvarez, Maria X. |
collection | PubMed |
description | Ruminants are a well-known reservoir for Listeria monocytogenes. In addition to asymptomatic carriage of the pathogen, ruminants can also acquire listeriosis and develop clinical manifestations in the form of neurologic or fetal infections, similar to those occurring in humans. Genomic characterization of ruminant listeriosis cases in Europe have identified lineage 1 and 2 strains associated with infection, as well as clonal complexes (CCs) that are commonly isolated from human cases of listeriosis; however, there is little information on the diversity of L. monocytogenes from ruminant listeriosis in the United States. In this study, we characterized and compared 73 L. monocytogenes isolates from ruminant listeriosis cases from the Midwest and the Upper Great Plains collected from 2015 to 2020. Using whole-genome sequence data, we classified the isolates and identified key virulence factors, stress-associated genes, and mobile genetic elements within our data set. Our isolates belonged to three different lineages: 31% to lineage 1, 53% to lineage 2, and 15% to lineage 3. Lineage 1 and 3 isolates were associated with neurologic infections, while lineage 2 showed a greater frequency of fetal infections. Additionally, the presence of mobile elements, virulence-associated genes, and stress and antimicrobial resistance genes was evaluated. These genetic elements are responsible for most of the subgroup-specific features and may play a key role in the spread of hypervirulent clones, including the spread of hypervirulent CC1 clone commonly associated with disease in humans, and may explain the increased frequency of certain clones in the area. IMPORTANCE Listeria monocytogenes affects humans and animals, causing encephalitis, septicemia, and abortions, among other clinical outcomes. Ruminants such as cattle, goats, and sheep are the main carriers contributing to the maintenance and dispersal of this pathogen in the farm environment. Contamination of food products from farms is of concern not only because many L. monocytogenes genotypes found there are associated with human listeriosis but also as a cause of significant economic losses when livestock and food products are affected. Ruminant listeriosis has been characterized extensively in Europe; however, there is limited information about the genetic diversity of these cases in the United States. Identification of subgroups with a greater ability to spread may facilitate surveillance and management of listeriosis and contribute to a better understanding of the genome diversity of this pathogen, providing insights into the molecular epidemiology of ruminant listeriosis in the region. |
format | Online Article Text |
id | pubmed-9769944 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-97699442022-12-22 Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States Cardenas-Alvarez, Maria X. Zeng, Hui Webb, Brett T. Mani, Rinosh Muñoz, Marina Bergholz, Teresa M. Microbiol Spectr Research Article Ruminants are a well-known reservoir for Listeria monocytogenes. In addition to asymptomatic carriage of the pathogen, ruminants can also acquire listeriosis and develop clinical manifestations in the form of neurologic or fetal infections, similar to those occurring in humans. Genomic characterization of ruminant listeriosis cases in Europe have identified lineage 1 and 2 strains associated with infection, as well as clonal complexes (CCs) that are commonly isolated from human cases of listeriosis; however, there is little information on the diversity of L. monocytogenes from ruminant listeriosis in the United States. In this study, we characterized and compared 73 L. monocytogenes isolates from ruminant listeriosis cases from the Midwest and the Upper Great Plains collected from 2015 to 2020. Using whole-genome sequence data, we classified the isolates and identified key virulence factors, stress-associated genes, and mobile genetic elements within our data set. Our isolates belonged to three different lineages: 31% to lineage 1, 53% to lineage 2, and 15% to lineage 3. Lineage 1 and 3 isolates were associated with neurologic infections, while lineage 2 showed a greater frequency of fetal infections. Additionally, the presence of mobile elements, virulence-associated genes, and stress and antimicrobial resistance genes was evaluated. These genetic elements are responsible for most of the subgroup-specific features and may play a key role in the spread of hypervirulent clones, including the spread of hypervirulent CC1 clone commonly associated with disease in humans, and may explain the increased frequency of certain clones in the area. IMPORTANCE Listeria monocytogenes affects humans and animals, causing encephalitis, septicemia, and abortions, among other clinical outcomes. Ruminants such as cattle, goats, and sheep are the main carriers contributing to the maintenance and dispersal of this pathogen in the farm environment. Contamination of food products from farms is of concern not only because many L. monocytogenes genotypes found there are associated with human listeriosis but also as a cause of significant economic losses when livestock and food products are affected. Ruminant listeriosis has been characterized extensively in Europe; however, there is limited information about the genetic diversity of these cases in the United States. Identification of subgroups with a greater ability to spread may facilitate surveillance and management of listeriosis and contribute to a better understanding of the genome diversity of this pathogen, providing insights into the molecular epidemiology of ruminant listeriosis in the region. American Society for Microbiology 2022-10-31 /pmc/articles/PMC9769944/ /pubmed/36314928 http://dx.doi.org/10.1128/spectrum.01579-22 Text en Copyright © 2022 Cardenas-Alvarez et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Cardenas-Alvarez, Maria X. Zeng, Hui Webb, Brett T. Mani, Rinosh Muñoz, Marina Bergholz, Teresa M. Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States |
title | Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States |
title_full | Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States |
title_fullStr | Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States |
title_full_unstemmed | Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States |
title_short | Comparative Genomics of Listeria monocytogenes Isolates from Ruminant Listeriosis Cases in the Midwest United States |
title_sort | comparative genomics of listeria monocytogenes isolates from ruminant listeriosis cases in the midwest united states |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769944/ https://www.ncbi.nlm.nih.gov/pubmed/36314928 http://dx.doi.org/10.1128/spectrum.01579-22 |
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