Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa

Bloodstream infections caused by nontyphoidal Salmonella are a major public health concern in Africa, causing ~49,600 deaths every year. The most common Salmonella enterica pathovariant associated with invasive nontyphoidal Salmonella disease is Salmonella Typhimurium sequence type (ST)313. It has b...

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Autores principales: Pulford, Caisey V., Perez-Sepulveda, Blanca M., Canals, Rocío, Bevington, Jessica A., Bengtsson, Rebecca J., Wenner, Nicolas, Rodwell, Ella V., Kumwenda, Benjamin, Zhu, Xiaojun, Bennett, Rebecca J., Stenhouse, George E., Malaka De Silva, P., Webster, Hermione J., Bengoechea, Jose A., Dumigan, Amy, Tran-Dien, Alicia, Prakash, Reenesh, Banda, Happy C., Alufandika, Lovemore, Mautanga, Mike P., Bowers-Barnard, Arthur, Beliavskaia, Alexandra Y., Predeus, Alexander V., Rowe, Will P. M., Darby, Alistair C., Hall, Neil, Weill, François-Xavier, Gordon, Melita A., Feasey, Nicholas A., Baker, Kate S., Hinton, Jay C. D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8018540/
https://www.ncbi.nlm.nih.gov/pubmed/33349664
http://dx.doi.org/10.1038/s41564-020-00836-1
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author Pulford, Caisey V.
Perez-Sepulveda, Blanca M.
Canals, Rocío
Bevington, Jessica A.
Bengtsson, Rebecca J.
Wenner, Nicolas
Rodwell, Ella V.
Kumwenda, Benjamin
Zhu, Xiaojun
Bennett, Rebecca J.
Stenhouse, George E.
Malaka De Silva, P.
Webster, Hermione J.
Bengoechea, Jose A.
Dumigan, Amy
Tran-Dien, Alicia
Prakash, Reenesh
Banda, Happy C.
Alufandika, Lovemore
Mautanga, Mike P.
Bowers-Barnard, Arthur
Beliavskaia, Alexandra Y.
Predeus, Alexander V.
Rowe, Will P. M.
Darby, Alistair C.
Hall, Neil
Weill, François-Xavier
Gordon, Melita A.
Feasey, Nicholas A.
Baker, Kate S.
Hinton, Jay C. D.
author_facet Pulford, Caisey V.
Perez-Sepulveda, Blanca M.
Canals, Rocío
Bevington, Jessica A.
Bengtsson, Rebecca J.
Wenner, Nicolas
Rodwell, Ella V.
Kumwenda, Benjamin
Zhu, Xiaojun
Bennett, Rebecca J.
Stenhouse, George E.
Malaka De Silva, P.
Webster, Hermione J.
Bengoechea, Jose A.
Dumigan, Amy
Tran-Dien, Alicia
Prakash, Reenesh
Banda, Happy C.
Alufandika, Lovemore
Mautanga, Mike P.
Bowers-Barnard, Arthur
Beliavskaia, Alexandra Y.
Predeus, Alexander V.
Rowe, Will P. M.
Darby, Alistair C.
Hall, Neil
Weill, François-Xavier
Gordon, Melita A.
Feasey, Nicholas A.
Baker, Kate S.
Hinton, Jay C. D.
author_sort Pulford, Caisey V.
collection PubMed
description Bloodstream infections caused by nontyphoidal Salmonella are a major public health concern in Africa, causing ~49,600 deaths every year. The most common Salmonella enterica pathovariant associated with invasive nontyphoidal Salmonella disease is Salmonella Typhimurium sequence type (ST)313. It has been proposed that antimicrobial resistance and genome degradation has contributed to the success of ST313 lineages in Africa, but the evolutionary trajectory of such changes was unclear. Here, to define the evolutionary dynamics of ST313, we sub-sampled from two comprehensive collections of Salmonella isolates from African patients with bloodstream infections, spanning 1966 to 2018. The resulting 680 genome sequences led to the discovery of a pan-susceptible ST313 lineage (ST313 L3), which emerged in Malawi in 2016 and is closely related to ST313 variants that cause gastrointestinal disease in the United Kingdom and Brazil. Genomic analysis revealed degradation events in important virulence genes in ST313 L3, which had not occurred in other ST313 lineages. Despite arising only recently in the clinic, ST313 L3 is a phylogenetic intermediate between ST313 L1 and L2, with a characteristic accessory genome. Our in-depth genotypic and phenotypic characterization identifies the crucial loss-of-function genetic events that occurred during the stepwise evolution of invasive S. Typhimurium across Africa.
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spelling pubmed-80185402021-04-16 Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa Pulford, Caisey V. Perez-Sepulveda, Blanca M. Canals, Rocío Bevington, Jessica A. Bengtsson, Rebecca J. Wenner, Nicolas Rodwell, Ella V. Kumwenda, Benjamin Zhu, Xiaojun Bennett, Rebecca J. Stenhouse, George E. Malaka De Silva, P. Webster, Hermione J. Bengoechea, Jose A. Dumigan, Amy Tran-Dien, Alicia Prakash, Reenesh Banda, Happy C. Alufandika, Lovemore Mautanga, Mike P. Bowers-Barnard, Arthur Beliavskaia, Alexandra Y. Predeus, Alexander V. Rowe, Will P. M. Darby, Alistair C. Hall, Neil Weill, François-Xavier Gordon, Melita A. Feasey, Nicholas A. Baker, Kate S. Hinton, Jay C. D. Nat Microbiol Article Bloodstream infections caused by nontyphoidal Salmonella are a major public health concern in Africa, causing ~49,600 deaths every year. The most common Salmonella enterica pathovariant associated with invasive nontyphoidal Salmonella disease is Salmonella Typhimurium sequence type (ST)313. It has been proposed that antimicrobial resistance and genome degradation has contributed to the success of ST313 lineages in Africa, but the evolutionary trajectory of such changes was unclear. Here, to define the evolutionary dynamics of ST313, we sub-sampled from two comprehensive collections of Salmonella isolates from African patients with bloodstream infections, spanning 1966 to 2018. The resulting 680 genome sequences led to the discovery of a pan-susceptible ST313 lineage (ST313 L3), which emerged in Malawi in 2016 and is closely related to ST313 variants that cause gastrointestinal disease in the United Kingdom and Brazil. Genomic analysis revealed degradation events in important virulence genes in ST313 L3, which had not occurred in other ST313 lineages. Despite arising only recently in the clinic, ST313 L3 is a phylogenetic intermediate between ST313 L1 and L2, with a characteristic accessory genome. Our in-depth genotypic and phenotypic characterization identifies the crucial loss-of-function genetic events that occurred during the stepwise evolution of invasive S. Typhimurium across Africa. Nature Publishing Group UK 2020-12-21 2021 /pmc/articles/PMC8018540/ /pubmed/33349664 http://dx.doi.org/10.1038/s41564-020-00836-1 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Pulford, Caisey V.
Perez-Sepulveda, Blanca M.
Canals, Rocío
Bevington, Jessica A.
Bengtsson, Rebecca J.
Wenner, Nicolas
Rodwell, Ella V.
Kumwenda, Benjamin
Zhu, Xiaojun
Bennett, Rebecca J.
Stenhouse, George E.
Malaka De Silva, P.
Webster, Hermione J.
Bengoechea, Jose A.
Dumigan, Amy
Tran-Dien, Alicia
Prakash, Reenesh
Banda, Happy C.
Alufandika, Lovemore
Mautanga, Mike P.
Bowers-Barnard, Arthur
Beliavskaia, Alexandra Y.
Predeus, Alexander V.
Rowe, Will P. M.
Darby, Alistair C.
Hall, Neil
Weill, François-Xavier
Gordon, Melita A.
Feasey, Nicholas A.
Baker, Kate S.
Hinton, Jay C. D.
Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa
title Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa
title_full Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa
title_fullStr Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa
title_full_unstemmed Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa
title_short Stepwise evolution of Salmonella Typhimurium ST313 causing bloodstream infection in Africa
title_sort stepwise evolution of salmonella typhimurium st313 causing bloodstream infection in africa
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8018540/
https://www.ncbi.nlm.nih.gov/pubmed/33349664
http://dx.doi.org/10.1038/s41564-020-00836-1
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