ICEmST contributes to colonization of Salmonella in the intestine of piglets

Abstract Salmonella enterica serovar 4,[5],12:i:- sequence type 34 (ST34) has recently become a global concern for public and animal health. The acquisition of mobile genetic element ICEmST, which contains two copper tolerance gene clusters, cus and pco, influences the epidemic success of this clone...

Full description

Saved in:
Bibliographic Details
Main Authors: Nobuo Arai, Tomoyuki Shibahara, Reina Nishiura, Yukino Tamamura-Andoh, Hayate Nishiura, Yoshihiro Muneta, Hiroshi Sawada, Ayako Watanabe-Yanai, Taketoshi Iwata, Masato Akiba, Masahiro Kusumoto
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-024-83039-6
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850102991209627648
author Nobuo Arai
Tomoyuki Shibahara
Reina Nishiura
Yukino Tamamura-Andoh
Hayate Nishiura
Yoshihiro Muneta
Hiroshi Sawada
Ayako Watanabe-Yanai
Taketoshi Iwata
Masato Akiba
Masahiro Kusumoto
author_facet Nobuo Arai
Tomoyuki Shibahara
Reina Nishiura
Yukino Tamamura-Andoh
Hayate Nishiura
Yoshihiro Muneta
Hiroshi Sawada
Ayako Watanabe-Yanai
Taketoshi Iwata
Masato Akiba
Masahiro Kusumoto
author_sort Nobuo Arai
collection DOAJ
description Abstract Salmonella enterica serovar 4,[5],12:i:- sequence type 34 (ST34) has recently become a global concern for public and animal health. The acquisition of mobile genetic element ICEmST, which contains two copper tolerance gene clusters, cus and pco, influences the epidemic success of this clone. Copper is used as a feed additive in swine at levels that potentially lead to selection pressure for Enterobacteriaceae; however, it remains unclear whether the copper tolerance system of ICEmST functions in vivo. We performed competition assays with Salmonella 4,[5],12:i:- ST34 wildtype (WT) and deletion mutants of ICEmST (ΔICEmST, Δcus, and Δpco) in groups of mice fed 0, 150, and 500 ppm CuSO4. In the competition of WT against ΔICEmST and Δcus, the competitive index of the 500 ppm-fed group was significantly lower than that of the 0 ppm-fed group. In the swine experiment, all individuals were fed 150 ppm CuSO4. The number of ICEmST-positive strain in the feces was significantly greater than that of ICEmST-negative strain. The serum inflammatory markers were significantly increased in swine infected with the ICEmST-positive strain. These data suggest that ICEmST, especially cus, provides Salmonella with the ability to colonize in the intestine, even at high copper concentrations, leading to swine salmonellosis.
format Article
id doaj-art-2c3beb233fe34b83a3344b695a4db418
institution DOAJ
issn 2045-2322
language English
publishDate 2024-12-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-2c3beb233fe34b83a3344b695a4db4182025-08-20T02:39:38ZengNature PortfolioScientific Reports2045-23222024-12-0114111010.1038/s41598-024-83039-6ICEmST contributes to colonization of Salmonella in the intestine of pigletsNobuo Arai0Tomoyuki Shibahara1Reina Nishiura2Yukino Tamamura-Andoh3Hayate Nishiura4Yoshihiro Muneta5Hiroshi Sawada6Ayako Watanabe-Yanai7Taketoshi Iwata8Masato Akiba9Masahiro Kusumoto10Division of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Hygiene Management Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Hygiene Management Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Hygiene Management Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Hygiene Management Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationDivision of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationLaboratory of Veterinary Bacteriology, School of Veterinary Medicine, Rakuno Gakuen UniversityDivision of Zoonosis Research, National Institute of Animal Health, National Agriculture and Food Research OrganizationAbstract Salmonella enterica serovar 4,[5],12:i:- sequence type 34 (ST34) has recently become a global concern for public and animal health. The acquisition of mobile genetic element ICEmST, which contains two copper tolerance gene clusters, cus and pco, influences the epidemic success of this clone. Copper is used as a feed additive in swine at levels that potentially lead to selection pressure for Enterobacteriaceae; however, it remains unclear whether the copper tolerance system of ICEmST functions in vivo. We performed competition assays with Salmonella 4,[5],12:i:- ST34 wildtype (WT) and deletion mutants of ICEmST (ΔICEmST, Δcus, and Δpco) in groups of mice fed 0, 150, and 500 ppm CuSO4. In the competition of WT against ΔICEmST and Δcus, the competitive index of the 500 ppm-fed group was significantly lower than that of the 0 ppm-fed group. In the swine experiment, all individuals were fed 150 ppm CuSO4. The number of ICEmST-positive strain in the feces was significantly greater than that of ICEmST-negative strain. The serum inflammatory markers were significantly increased in swine infected with the ICEmST-positive strain. These data suggest that ICEmST, especially cus, provides Salmonella with the ability to colonize in the intestine, even at high copper concentrations, leading to swine salmonellosis.https://doi.org/10.1038/s41598-024-83039-6Copper toleranceFeedICEmSTSalmonella 4,[5],12:i:-Swine
spellingShingle Nobuo Arai
Tomoyuki Shibahara
Reina Nishiura
Yukino Tamamura-Andoh
Hayate Nishiura
Yoshihiro Muneta
Hiroshi Sawada
Ayako Watanabe-Yanai
Taketoshi Iwata
Masato Akiba
Masahiro Kusumoto
ICEmST contributes to colonization of Salmonella in the intestine of piglets
Scientific Reports
Copper tolerance
Feed
ICEmST
Salmonella 4,[5],12:i:-
Swine
title ICEmST contributes to colonization of Salmonella in the intestine of piglets
title_full ICEmST contributes to colonization of Salmonella in the intestine of piglets
title_fullStr ICEmST contributes to colonization of Salmonella in the intestine of piglets
title_full_unstemmed ICEmST contributes to colonization of Salmonella in the intestine of piglets
title_short ICEmST contributes to colonization of Salmonella in the intestine of piglets
title_sort icemst contributes to colonization of salmonella in the intestine of piglets
topic Copper tolerance
Feed
ICEmST
Salmonella 4,[5],12:i:-
Swine
url https://doi.org/10.1038/s41598-024-83039-6
work_keys_str_mv AT nobuoarai icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT tomoyukishibahara icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT reinanishiura icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT yukinotamamuraandoh icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT hayatenishiura icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT yoshihiromuneta icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT hiroshisawada icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT ayakowatanabeyanai icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT taketoshiiwata icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT masatoakiba icemstcontributestocolonizationofsalmonellaintheintestineofpiglets
AT masahirokusumoto icemstcontributestocolonizationofsalmonellaintheintestineofpiglets