Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan

ABSTRACT The continuous emergence of carbapenemase-producing Enterobacteriaceae (CPE) presents a great public health challenge. Mitigation of CPE spread in the environment is crucial, particularly from a One Health perspective. Here we describe the isolation of CPE strain SNI47 from influent water o...

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Autores principales:	Yasunori Suzuki, Miki Ida, Hiroaki Kubota, Tsukasa Ariyoshi, Ko Murakami, Makiko Kobayashi, Rei Kato, Akihiko Hirai, Jun Suzuki, Kenji Sadamasu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	carbapenemase-producing Enterobacteriaceae conjugal transfer metallo-β-lactamase plasmid whole-genome sequencing Enterobacteriaceae Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c44f2bb42cab4833a4273b5139a6fdff
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spelling	oai:doaj.org-article:c44f2bb42cab4833a4273b5139a6fdff2021-11-15T15:27:32ZMultiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan10.1128/mSphere.00391-192379-5042https://doaj.org/article/c44f2bb42cab4833a4273b5139a6fdff2019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00391-19https://doaj.org/toc/2379-5042ABSTRACT The continuous emergence of carbapenemase-producing Enterobacteriaceae (CPE) presents a great public health challenge. Mitigation of CPE spread in the environment is crucial, particularly from a One Health perspective. Here we describe the isolation of CPE strain SNI47 from influent water of a sewage treatment plant in Japan. SNI47 was identified as Klebsiella quasipneumoniae subsp. quasipneumoniae by phylogenetic analysis and was resistant to β-lactams, including carbapenems. Of four plasmids detected from SNI47, the 185,311-bp IncA/C2 plasmid (pTMSNI47-1), which carried 10 drug resistance genes, including genes for four β-lactamases (blaCTX-M-2, blaDHA-1, blaKHM-1, and blaOXA-10), was transferred to Escherichia coli J53 via conjugation. The MICs of all tested β-lactams for the transconjugant were higher than for the recipient. We constructed recombinant plasmids, into which each β-lactamase gene was inserted, and used them to transform E. coli DH5α cells, demonstrating that KHM-1 enhanced carbapenem resistance. In addition, these β-lactamases were responsible for a wide-spectrum β-lactam resistance acquisition with mutual compensation. KHM-1, recognized as a rare type of metallo-β-lactamase, was detected in a transferable plasmid, from a sewage treatment plant, involved in horizontal gene transfer. The detection of such plasmids raises a health risk alarm for CPE dissemination. IMPORTANCE In our investigation of urban wastewater in Japan, carbapenem-resistant Klebsiella quasipneumoniae subsp. quasipneumoniae was isolated that carried the pTMSNI47-1 plasmid, which carries four β-lactamase genes and has transferability among Enterobacteriaceae. pTMSNI47-1 was found to encode a rarely reported carbapenemase, KHM-1. Cooperative effects of β-lactamases encoded by pTMSNI47-1 appeared to have broad-spectrum resistance to β-lactams. The detection of the KHM-1 gene in urban wastewater suggests that such a rare antimicrobial resistance (AMR) gene can be pooled in the environment, potentially emerging as an AMR determinant in a pathogen. When the number of β-lactamase resistance genes is increased in one plasmid, the transfer of this plasmid can confer broad-spectrum resistance to β-lactams, even if the individual gene confers narrow-spectrum resistance. The present study adds important information about the potential risk of sewage treatment plants as reservoirs and environmental suppliers of AMR genes, contributing to the public health from a One Health perspective.Yasunori SuzukiMiki IdaHiroaki KubotaTsukasa AriyoshiKo MurakamiMakiko KobayashiRei KatoAkihiko HiraiJun SuzukiKenji SadamasuAmerican Society for Microbiologyarticlecarbapenemase-producing Enterobacteriaceaeconjugal transfermetallo-β-lactamaseplasmidwhole-genome sequencingEnterobacteriaceaeMicrobiologyQR1-502ENmSphere, Vol 4, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbapenemase-producing Enterobacteriaceae conjugal transfer metallo-β-lactamase plasmid whole-genome sequencing Enterobacteriaceae Microbiology QR1-502
spellingShingle	carbapenemase-producing Enterobacteriaceae conjugal transfer metallo-β-lactamase plasmid whole-genome sequencing Enterobacteriaceae Microbiology QR1-502 Yasunori Suzuki Miki Ida Hiroaki Kubota Tsukasa Ariyoshi Ko Murakami Makiko Kobayashi Rei Kato Akihiko Hirai Jun Suzuki Kenji Sadamasu Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan
description	ABSTRACT The continuous emergence of carbapenemase-producing Enterobacteriaceae (CPE) presents a great public health challenge. Mitigation of CPE spread in the environment is crucial, particularly from a One Health perspective. Here we describe the isolation of CPE strain SNI47 from influent water of a sewage treatment plant in Japan. SNI47 was identified as Klebsiella quasipneumoniae subsp. quasipneumoniae by phylogenetic analysis and was resistant to β-lactams, including carbapenems. Of four plasmids detected from SNI47, the 185,311-bp IncA/C2 plasmid (pTMSNI47-1), which carried 10 drug resistance genes, including genes for four β-lactamases (blaCTX-M-2, blaDHA-1, blaKHM-1, and blaOXA-10), was transferred to Escherichia coli J53 via conjugation. The MICs of all tested β-lactams for the transconjugant were higher than for the recipient. We constructed recombinant plasmids, into which each β-lactamase gene was inserted, and used them to transform E. coli DH5α cells, demonstrating that KHM-1 enhanced carbapenem resistance. In addition, these β-lactamases were responsible for a wide-spectrum β-lactam resistance acquisition with mutual compensation. KHM-1, recognized as a rare type of metallo-β-lactamase, was detected in a transferable plasmid, from a sewage treatment plant, involved in horizontal gene transfer. The detection of such plasmids raises a health risk alarm for CPE dissemination. IMPORTANCE In our investigation of urban wastewater in Japan, carbapenem-resistant Klebsiella quasipneumoniae subsp. quasipneumoniae was isolated that carried the pTMSNI47-1 plasmid, which carries four β-lactamase genes and has transferability among Enterobacteriaceae. pTMSNI47-1 was found to encode a rarely reported carbapenemase, KHM-1. Cooperative effects of β-lactamases encoded by pTMSNI47-1 appeared to have broad-spectrum resistance to β-lactams. The detection of the KHM-1 gene in urban wastewater suggests that such a rare antimicrobial resistance (AMR) gene can be pooled in the environment, potentially emerging as an AMR determinant in a pathogen. When the number of β-lactamase resistance genes is increased in one plasmid, the transfer of this plasmid can confer broad-spectrum resistance to β-lactams, even if the individual gene confers narrow-spectrum resistance. The present study adds important information about the potential risk of sewage treatment plants as reservoirs and environmental suppliers of AMR genes, contributing to the public health from a One Health perspective.
format	article
author	Yasunori Suzuki Miki Ida Hiroaki Kubota Tsukasa Ariyoshi Ko Murakami Makiko Kobayashi Rei Kato Akihiko Hirai Jun Suzuki Kenji Sadamasu
author_facet	Yasunori Suzuki Miki Ida Hiroaki Kubota Tsukasa Ariyoshi Ko Murakami Makiko Kobayashi Rei Kato Akihiko Hirai Jun Suzuki Kenji Sadamasu
author_sort	Yasunori Suzuki
title	Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan
title_short	Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan
title_full	Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan
title_fullStr	Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan
title_full_unstemmed	Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan
title_sort	multiple β-lactam resistance gene-carrying plasmid harbored by <named-content content-type="genus-species">klebsiella quasipneumoniae</named-content> isolated from urban sewage in japan
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/c44f2bb42cab4833a4273b5139a6fdff
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Multiple β-Lactam Resistance Gene-Carrying Plasmid Harbored by <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> Isolated from Urban Sewage in Japan

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