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Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region

In Japan’s Kanto region, the number of Salmonella enterica serovar Chester infections increased temporarily between 2014 and 2016. Concurrently with this temporal increase in the Kanto region, S. Chester isolates belonging to one clonal group were causing repetitive outbreaks in Europe. A recent stu...

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Autores principales: Ando, Naoshi, Sekizuka, Tsuyoshi, Yokoyama, Eiji, Aihara, Yoshiyuki, Konishi, Noriko, Matsumoto, Yuko, Ishida, Kumiko, Nagasawa, Koo, Jourdan-Da Silva, Nathalie, Suzuki, Motoi, Kimura, Hirokazu, Le Hello, Simon, Murakami, Koichi, Kuroda, Makoto, Hirai, Shinichiro, Fukaya, Setsuko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8354586/
https://www.ncbi.nlm.nih.gov/pubmed/34385991
http://dx.doi.org/10.3389/fmicb.2021.705679
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author Ando, Naoshi
Sekizuka, Tsuyoshi
Yokoyama, Eiji
Aihara, Yoshiyuki
Konishi, Noriko
Matsumoto, Yuko
Ishida, Kumiko
Nagasawa, Koo
Jourdan-Da Silva, Nathalie
Suzuki, Motoi
Kimura, Hirokazu
Le Hello, Simon
Murakami, Koichi
Kuroda, Makoto
Hirai, Shinichiro
Fukaya, Setsuko
author_facet Ando, Naoshi
Sekizuka, Tsuyoshi
Yokoyama, Eiji
Aihara, Yoshiyuki
Konishi, Noriko
Matsumoto, Yuko
Ishida, Kumiko
Nagasawa, Koo
Jourdan-Da Silva, Nathalie
Suzuki, Motoi
Kimura, Hirokazu
Le Hello, Simon
Murakami, Koichi
Kuroda, Makoto
Hirai, Shinichiro
Fukaya, Setsuko
author_sort Ando, Naoshi
collection PubMed
description In Japan’s Kanto region, the number of Salmonella enterica serovar Chester infections increased temporarily between 2014 and 2016. Concurrently with this temporal increase in the Kanto region, S. Chester isolates belonging to one clonal group were causing repetitive outbreaks in Europe. A recent study reported that the European outbreaks were associated with travelers who had been exposed to contaminated food in Morocco, possibly seafood. Because Japan imports a large amount of seafood from Morocco, we aimed to establish whether the temporal increase in S. Chester infections in the Kanto region was associated with imported Moroccan seafood. Short sequence reads from the whole-genome sequencing of 47 S. Chester isolates from people in the Kanto region (2014–2016), and the additional genome sequences from 58 isolates from the European outbreaks, were analyzed. The reads were compared with the complete genome sequence from a S. Chester reference strain, and 347 single nucleotide polymorphisms (SNPs) were identified. These SNPs were used in this study. Cluster and Bayesian cluster analyses showed that the Japanese and European isolates fell into two different clusters. Therefore, Φ(PT) and [Formula: see text] values were calculated to evaluate genetic differences between these clusters. The results revealed that the Japanese and European isolates were genetically distinct populations. Our root-to-tip analysis showed that the Japanese isolates originating from one clone had accumulated mutations, suggesting that an emergence of this organism occurred. A minimum spanning tree analysis demonstrated no correlation between genetic and geographical distances in the Japanese isolates, suggesting that the emergence of the serovar in the Kanto region did not involve person-to-person contact; rather, it occurred through food consumption. The d(N)/d(S) ratio indicated that the Japanese strain has evolved under positive selection pressure. Generally, a population of bacterial clones in a reservoir faces negative selection pressure. Therefore, the Japanese strain must have existed outside of any reservoir during its emergence. In conclusion, S. Chester isolates originating from one clone probably emerged in the Kanto region via the consumption of contaminated foods other than imported Moroccan seafood. The emerging strain may have not established a reservoir for survival in the food supply chain resulting in its disappearance after 2017.
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spelling pubmed-83545862021-08-11 Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region Ando, Naoshi Sekizuka, Tsuyoshi Yokoyama, Eiji Aihara, Yoshiyuki Konishi, Noriko Matsumoto, Yuko Ishida, Kumiko Nagasawa, Koo Jourdan-Da Silva, Nathalie Suzuki, Motoi Kimura, Hirokazu Le Hello, Simon Murakami, Koichi Kuroda, Makoto Hirai, Shinichiro Fukaya, Setsuko Front Microbiol Microbiology In Japan’s Kanto region, the number of Salmonella enterica serovar Chester infections increased temporarily between 2014 and 2016. Concurrently with this temporal increase in the Kanto region, S. Chester isolates belonging to one clonal group were causing repetitive outbreaks in Europe. A recent study reported that the European outbreaks were associated with travelers who had been exposed to contaminated food in Morocco, possibly seafood. Because Japan imports a large amount of seafood from Morocco, we aimed to establish whether the temporal increase in S. Chester infections in the Kanto region was associated with imported Moroccan seafood. Short sequence reads from the whole-genome sequencing of 47 S. Chester isolates from people in the Kanto region (2014–2016), and the additional genome sequences from 58 isolates from the European outbreaks, were analyzed. The reads were compared with the complete genome sequence from a S. Chester reference strain, and 347 single nucleotide polymorphisms (SNPs) were identified. These SNPs were used in this study. Cluster and Bayesian cluster analyses showed that the Japanese and European isolates fell into two different clusters. Therefore, Φ(PT) and [Formula: see text] values were calculated to evaluate genetic differences between these clusters. The results revealed that the Japanese and European isolates were genetically distinct populations. Our root-to-tip analysis showed that the Japanese isolates originating from one clone had accumulated mutations, suggesting that an emergence of this organism occurred. A minimum spanning tree analysis demonstrated no correlation between genetic and geographical distances in the Japanese isolates, suggesting that the emergence of the serovar in the Kanto region did not involve person-to-person contact; rather, it occurred through food consumption. The d(N)/d(S) ratio indicated that the Japanese strain has evolved under positive selection pressure. Generally, a population of bacterial clones in a reservoir faces negative selection pressure. Therefore, the Japanese strain must have existed outside of any reservoir during its emergence. In conclusion, S. Chester isolates originating from one clone probably emerged in the Kanto region via the consumption of contaminated foods other than imported Moroccan seafood. The emerging strain may have not established a reservoir for survival in the food supply chain resulting in its disappearance after 2017. Frontiers Media S.A. 2021-07-27 /pmc/articles/PMC8354586/ /pubmed/34385991 http://dx.doi.org/10.3389/fmicb.2021.705679 Text en Copyright © 2021 Ando, Sekizuka, Yokoyama, Aihara, Konishi, Matsumoto, Ishida, Nagasawa, Jourdan-Da Silva, Suzuki, Kimura, Le Hello, Murakami, Kuroda, Hirai and Fukaya. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ando, Naoshi
Sekizuka, Tsuyoshi
Yokoyama, Eiji
Aihara, Yoshiyuki
Konishi, Noriko
Matsumoto, Yuko
Ishida, Kumiko
Nagasawa, Koo
Jourdan-Da Silva, Nathalie
Suzuki, Motoi
Kimura, Hirokazu
Le Hello, Simon
Murakami, Koichi
Kuroda, Makoto
Hirai, Shinichiro
Fukaya, Setsuko
Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region
title Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region
title_full Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region
title_fullStr Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region
title_full_unstemmed Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region
title_short Whole Genome Analysis Detects the Emergence of a Single Salmonella enterica Serovar Chester Clone in Japan’s Kanto Region
title_sort whole genome analysis detects the emergence of a single salmonella enterica serovar chester clone in japan’s kanto region
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8354586/
https://www.ncbi.nlm.nih.gov/pubmed/34385991
http://dx.doi.org/10.3389/fmicb.2021.705679
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