Evolution and population structure of Salmonella enterica serovar Newport

Vartul Sangal, Heather Harbottle, Camila Mazzoni, Reiner Helmuth, Beatriz Guerra, Xavier Didelot, Bianca Paglietti, Wolfgang Rabsch, Sylvain Brisse, François-Xavier Weill, Philippe Roumagnac, Mark Achtman

Research output: Contribution to journalArticle

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Abstract

Salmonellosis caused by Salmonella enterica serovar Newport is a major global public health concern, particularly because S. Newport isolates that are resistant to multiple drugs (MDR), including third-generation cephalosporins (MDR-AmpC phenotype), have been commonly isolated from food animals. We analyzed 384 S. Newport isolates from various sources by a multilocus sequence typing (MLST) scheme to study the evolution and population structure of the serovar. These were compared to the population structure of S. enterica serovars Enteritidis, Kentucky, Paratyphi B, and Typhimurium. Our S. Newport collection fell into three lineages, Newport-I, Newport-II, and Newport-III, each of which contained multiple sequence types (STs). Newport-I has only a few STs, unlike Newport-II or Newport-III, and has possibly emerged recently. Newport-I is more prevalent among humans in Europe than in North America, whereas Newport-II is preferentially associated with animals. Two STs of Newport-II encompassed all MDR-AmpC isolates, suggesting recent global spread after the acquisition of the blaCMY-2 gene. In contrast, most Newport-III isolates were from humans in North America and were pansusceptible to antibiotics. Newport was intermediate in population structure to the other serovars, which varied from a single monophyletic lineage in S. Enteritidis or S. Typhimurium to four discrete lineages within S. Paratyphi B. Both mutation and homologous recombination are responsible for diversification within each of these lineages, but the relative frequencies differed with the lineage. We conclude that serovars of S. enterica provide a variety of different population structures.
LanguageEnglish
Pages6465-6476
Number of pages12
JournalJournal of Bacteriology
Volume192
Issue number24
DOIs
Publication statusPublished - 2010

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Salmonella enterica
North America
Population
Pharmaceutical Preparations
Multilocus Sequence Typing
Salmonella enteritidis
Salmonella Infections
Homologous Recombination
Cephalosporins
Public Health
Anti-Bacterial Agents
Phenotype
Food
Mutation
Serogroup
Genes

Keywords

  • population structure
  • salmonella enterica

Cite this

Sangal, V., Harbottle, H., Mazzoni, C., Helmuth, R., Guerra, B., Didelot, X., ... Achtman, M. (2010). Evolution and population structure of Salmonella enterica serovar Newport. Journal of Bacteriology, 192(24), 6465-6476. https://doi.org/10.1128/​JB.00969-10
Sangal, Vartul ; Harbottle, Heather ; Mazzoni, Camila ; Helmuth, Reiner ; Guerra, Beatriz ; Didelot, Xavier ; Paglietti, Bianca ; Rabsch, Wolfgang ; Brisse, Sylvain ; Weill, François-Xavier ; Roumagnac, Philippe ; Achtman, Mark. / Evolution and population structure of Salmonella enterica serovar Newport. In: Journal of Bacteriology. 2010 ; Vol. 192, No. 24. pp. 6465-6476.
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abstract = "Salmonellosis caused by Salmonella enterica serovar Newport is a major global public health concern, particularly because S. Newport isolates that are resistant to multiple drugs (MDR), including third-generation cephalosporins (MDR-AmpC phenotype), have been commonly isolated from food animals. We analyzed 384 S. Newport isolates from various sources by a multilocus sequence typing (MLST) scheme to study the evolution and population structure of the serovar. These were compared to the population structure of S. enterica serovars Enteritidis, Kentucky, Paratyphi B, and Typhimurium. Our S. Newport collection fell into three lineages, Newport-I, Newport-II, and Newport-III, each of which contained multiple sequence types (STs). Newport-I has only a few STs, unlike Newport-II or Newport-III, and has possibly emerged recently. Newport-I is more prevalent among humans in Europe than in North America, whereas Newport-II is preferentially associated with animals. Two STs of Newport-II encompassed all MDR-AmpC isolates, suggesting recent global spread after the acquisition of the blaCMY-2 gene. In contrast, most Newport-III isolates were from humans in North America and were pansusceptible to antibiotics. Newport was intermediate in population structure to the other serovars, which varied from a single monophyletic lineage in S. Enteritidis or S. Typhimurium to four discrete lineages within S. Paratyphi B. Both mutation and homologous recombination are responsible for diversification within each of these lineages, but the relative frequencies differed with the lineage. We conclude that serovars of S. enterica provide a variety of different population structures.",
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Sangal, V, Harbottle, H, Mazzoni, C, Helmuth, R, Guerra, B, Didelot, X, Paglietti, B, Rabsch, W, Brisse, S, Weill, F-X, Roumagnac, P & Achtman, M 2010, 'Evolution and population structure of Salmonella enterica serovar Newport' Journal of Bacteriology, vol. 192, no. 24, pp. 6465-6476. https://doi.org/10.1128/​JB.00969-10

Evolution and population structure of Salmonella enterica serovar Newport. / Sangal, Vartul; Harbottle, Heather; Mazzoni, Camila; Helmuth, Reiner; Guerra, Beatriz; Didelot, Xavier; Paglietti, Bianca; Rabsch, Wolfgang; Brisse, Sylvain ; Weill, François-Xavier ; Roumagnac, Philippe ; Achtman, Mark.

In: Journal of Bacteriology, Vol. 192, No. 24, 2010, p. 6465-6476.

Research output: Contribution to journalArticle

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T1 - Evolution and population structure of Salmonella enterica serovar Newport

AU - Sangal, Vartul

AU - Harbottle, Heather

AU - Mazzoni, Camila

AU - Helmuth, Reiner

AU - Guerra, Beatriz

AU - Didelot, Xavier

AU - Paglietti, Bianca

AU - Rabsch, Wolfgang

AU - Brisse, Sylvain

AU - Weill, François-Xavier

AU - Roumagnac, Philippe

AU - Achtman, Mark

PY - 2010

Y1 - 2010

N2 - Salmonellosis caused by Salmonella enterica serovar Newport is a major global public health concern, particularly because S. Newport isolates that are resistant to multiple drugs (MDR), including third-generation cephalosporins (MDR-AmpC phenotype), have been commonly isolated from food animals. We analyzed 384 S. Newport isolates from various sources by a multilocus sequence typing (MLST) scheme to study the evolution and population structure of the serovar. These were compared to the population structure of S. enterica serovars Enteritidis, Kentucky, Paratyphi B, and Typhimurium. Our S. Newport collection fell into three lineages, Newport-I, Newport-II, and Newport-III, each of which contained multiple sequence types (STs). Newport-I has only a few STs, unlike Newport-II or Newport-III, and has possibly emerged recently. Newport-I is more prevalent among humans in Europe than in North America, whereas Newport-II is preferentially associated with animals. Two STs of Newport-II encompassed all MDR-AmpC isolates, suggesting recent global spread after the acquisition of the blaCMY-2 gene. In contrast, most Newport-III isolates were from humans in North America and were pansusceptible to antibiotics. Newport was intermediate in population structure to the other serovars, which varied from a single monophyletic lineage in S. Enteritidis or S. Typhimurium to four discrete lineages within S. Paratyphi B. Both mutation and homologous recombination are responsible for diversification within each of these lineages, but the relative frequencies differed with the lineage. We conclude that serovars of S. enterica provide a variety of different population structures.

AB - Salmonellosis caused by Salmonella enterica serovar Newport is a major global public health concern, particularly because S. Newport isolates that are resistant to multiple drugs (MDR), including third-generation cephalosporins (MDR-AmpC phenotype), have been commonly isolated from food animals. We analyzed 384 S. Newport isolates from various sources by a multilocus sequence typing (MLST) scheme to study the evolution and population structure of the serovar. These were compared to the population structure of S. enterica serovars Enteritidis, Kentucky, Paratyphi B, and Typhimurium. Our S. Newport collection fell into three lineages, Newport-I, Newport-II, and Newport-III, each of which contained multiple sequence types (STs). Newport-I has only a few STs, unlike Newport-II or Newport-III, and has possibly emerged recently. Newport-I is more prevalent among humans in Europe than in North America, whereas Newport-II is preferentially associated with animals. Two STs of Newport-II encompassed all MDR-AmpC isolates, suggesting recent global spread after the acquisition of the blaCMY-2 gene. In contrast, most Newport-III isolates were from humans in North America and were pansusceptible to antibiotics. Newport was intermediate in population structure to the other serovars, which varied from a single monophyletic lineage in S. Enteritidis or S. Typhimurium to four discrete lineages within S. Paratyphi B. Both mutation and homologous recombination are responsible for diversification within each of these lineages, but the relative frequencies differed with the lineage. We conclude that serovars of S. enterica provide a variety of different population structures.

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KW - salmonella enterica

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DO - 10.1128/​JB.00969-10

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Sangal V, Harbottle H, Mazzoni C, Helmuth R, Guerra B, Didelot X et al. Evolution and population structure of Salmonella enterica serovar Newport. Journal of Bacteriology. 2010;192(24):6465-6476. https://doi.org/10.1128/​JB.00969-10