Jouman W Hassan, Tongzhou Xu, Marwan Osman, Steven J Schiff, David Mann, Xiangyu Deng, Jeffrey T LeJeune, Issmat I Kassem
{"title":"可传播的流动粘菌素耐药基因mcr-3和mcr-9经由进口海产品传入美国。","authors":"Jouman W Hassan, Tongzhou Xu, Marwan Osman, Steven J Schiff, David Mann, Xiangyu Deng, Jeffrey T LeJeune, Issmat I Kassem","doi":"10.1128/msphere.00253-25","DOIUrl":null,"url":null,"abstract":"<p><p>The emergence and global dissemination of the mobile colistin resistance genes (<i>mcr</i>) threaten the efficacy of colistin, a high-priority, critically important antibiotic that is used to treat complicated infections with multidrug-resistant Gram-negative bacteria in humans. The occurrence of <i>mcr</i> in the USA has been suggested to be relatively limited, particularly in bacteria associated with domestic foods and food animals. This is because colistin has neither been marketed nor approved for use in agriculture in the USA. However, <i>mcr</i>-carrying bacteria can occur on foods imported from countries where these genes might be relatively more prevalent. Yet, studies on <i>mcr</i> in vulnerable imported foods in the USA are lacking. To address this gap in knowledge, we assessed the role of imported seafood as a potential carrier of <i>mcr</i> genes to the USA. Imported seafood samples were aseptically collected from eight major retail stores across Georgia, USA. In-depth analyses revealed the occurrence of <i>mcr-9</i> in bacteria isolated from imported shrimp samples. The <i>mcr-9</i>-carrying bacteria were identified as <i>Serratia nevei</i>, a newly described species that belongs to the <i>Serratia marcescens</i> complex. The <i>mcr-9</i> in the <i>S. nevei</i> isolates was carried on IncHI2 plasmids that were transferable and conferred colistin resistance to naïve <i>Escherichia coli</i>. Further analysis identified a chromosomal <i>mcr-3.17</i> in <i>Aeromonas salmonicida</i> isolated from imported scallops. All the <i>mcr</i>-carrying isolates harbored other important antibiotic resistance genes. Taken together, our data showed that imported seafood, specifically shrimps, might be an overlooked source contributing to the introduction and spread of transmissible colistin resistance genes in the USA.</p><p><strong>Importance: </strong>Colistin, an important antibiotic, is used to treat certain bacterial infections in humans that can be severe and/or life-threatening. However, these bacteria can acquire the mobile colistin resistance (<i>mcr</i>) genes and become resistant to this antibiotic. Plasmid-borne <i>mcr</i> can jump between bacterial species, spreading in bacteria across a variety of hosts and niches. Therefore, monitoring the spread of <i>mcr</i> is critical to maintain the efficacy of colistin. In the USA, the occurrence of <i>mcr</i> in domestically produced food is thought to be limited. In this study, we showed that <i>mcr</i> can be carried into the USA by bacteria on imported seafood. A specific gene, <i>mcr-9</i>, was located on a plasmid that could be transferred to other bacteria. Therefore, imported seafood can be an overlooked source of <i>mcr</i> in the USA. It is important to monitor and assess <i>mcr</i> in imported seafood to control the proliferation of colistin resistance in the USA.</p>","PeriodicalId":19052,"journal":{"name":"mSphere","volume":" ","pages":"e0025325"},"PeriodicalIF":3.7000,"publicationDate":"2025-07-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Introduction of the transmissible mobile colistin resistance genes <i>mcr-3</i> and <i>mcr-9</i> to the USA via imported seafood.\",\"authors\":\"Jouman W Hassan, Tongzhou Xu, Marwan Osman, Steven J Schiff, David Mann, Xiangyu Deng, Jeffrey T LeJeune, Issmat I Kassem\",\"doi\":\"10.1128/msphere.00253-25\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The emergence and global dissemination of the mobile colistin resistance genes (<i>mcr</i>) threaten the efficacy of colistin, a high-priority, critically important antibiotic that is used to treat complicated infections with multidrug-resistant Gram-negative bacteria in humans. The occurrence of <i>mcr</i> in the USA has been suggested to be relatively limited, particularly in bacteria associated with domestic foods and food animals. This is because colistin has neither been marketed nor approved for use in agriculture in the USA. However, <i>mcr</i>-carrying bacteria can occur on foods imported from countries where these genes might be relatively more prevalent. Yet, studies on <i>mcr</i> in vulnerable imported foods in the USA are lacking. To address this gap in knowledge, we assessed the role of imported seafood as a potential carrier of <i>mcr</i> genes to the USA. Imported seafood samples were aseptically collected from eight major retail stores across Georgia, USA. In-depth analyses revealed the occurrence of <i>mcr-9</i> in bacteria isolated from imported shrimp samples. The <i>mcr-9</i>-carrying bacteria were identified as <i>Serratia nevei</i>, a newly described species that belongs to the <i>Serratia marcescens</i> complex. The <i>mcr-9</i> in the <i>S. nevei</i> isolates was carried on IncHI2 plasmids that were transferable and conferred colistin resistance to naïve <i>Escherichia coli</i>. Further analysis identified a chromosomal <i>mcr-3.17</i> in <i>Aeromonas salmonicida</i> isolated from imported scallops. All the <i>mcr</i>-carrying isolates harbored other important antibiotic resistance genes. Taken together, our data showed that imported seafood, specifically shrimps, might be an overlooked source contributing to the introduction and spread of transmissible colistin resistance genes in the USA.</p><p><strong>Importance: </strong>Colistin, an important antibiotic, is used to treat certain bacterial infections in humans that can be severe and/or life-threatening. However, these bacteria can acquire the mobile colistin resistance (<i>mcr</i>) genes and become resistant to this antibiotic. Plasmid-borne <i>mcr</i> can jump between bacterial species, spreading in bacteria across a variety of hosts and niches. Therefore, monitoring the spread of <i>mcr</i> is critical to maintain the efficacy of colistin. In the USA, the occurrence of <i>mcr</i> in domestically produced food is thought to be limited. In this study, we showed that <i>mcr</i> can be carried into the USA by bacteria on imported seafood. A specific gene, <i>mcr-9</i>, was located on a plasmid that could be transferred to other bacteria. Therefore, imported seafood can be an overlooked source of <i>mcr</i> in the USA. It is important to monitor and assess <i>mcr</i> in imported seafood to control the proliferation of colistin resistance in the USA.</p>\",\"PeriodicalId\":19052,\"journal\":{\"name\":\"mSphere\",\"volume\":\" \",\"pages\":\"e0025325\"},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2025-07-07\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"mSphere\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1128/msphere.00253-25\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"mSphere","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/msphere.00253-25","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
Introduction of the transmissible mobile colistin resistance genes mcr-3 and mcr-9 to the USA via imported seafood.
The emergence and global dissemination of the mobile colistin resistance genes (mcr) threaten the efficacy of colistin, a high-priority, critically important antibiotic that is used to treat complicated infections with multidrug-resistant Gram-negative bacteria in humans. The occurrence of mcr in the USA has been suggested to be relatively limited, particularly in bacteria associated with domestic foods and food animals. This is because colistin has neither been marketed nor approved for use in agriculture in the USA. However, mcr-carrying bacteria can occur on foods imported from countries where these genes might be relatively more prevalent. Yet, studies on mcr in vulnerable imported foods in the USA are lacking. To address this gap in knowledge, we assessed the role of imported seafood as a potential carrier of mcr genes to the USA. Imported seafood samples were aseptically collected from eight major retail stores across Georgia, USA. In-depth analyses revealed the occurrence of mcr-9 in bacteria isolated from imported shrimp samples. The mcr-9-carrying bacteria were identified as Serratia nevei, a newly described species that belongs to the Serratia marcescens complex. The mcr-9 in the S. nevei isolates was carried on IncHI2 plasmids that were transferable and conferred colistin resistance to naïve Escherichia coli. Further analysis identified a chromosomal mcr-3.17 in Aeromonas salmonicida isolated from imported scallops. All the mcr-carrying isolates harbored other important antibiotic resistance genes. Taken together, our data showed that imported seafood, specifically shrimps, might be an overlooked source contributing to the introduction and spread of transmissible colistin resistance genes in the USA.
Importance: Colistin, an important antibiotic, is used to treat certain bacterial infections in humans that can be severe and/or life-threatening. However, these bacteria can acquire the mobile colistin resistance (mcr) genes and become resistant to this antibiotic. Plasmid-borne mcr can jump between bacterial species, spreading in bacteria across a variety of hosts and niches. Therefore, monitoring the spread of mcr is critical to maintain the efficacy of colistin. In the USA, the occurrence of mcr in domestically produced food is thought to be limited. In this study, we showed that mcr can be carried into the USA by bacteria on imported seafood. A specific gene, mcr-9, was located on a plasmid that could be transferred to other bacteria. Therefore, imported seafood can be an overlooked source of mcr in the USA. It is important to monitor and assess mcr in imported seafood to control the proliferation of colistin resistance in the USA.
期刊介绍:
mSphere™ is a multi-disciplinary open-access journal that will focus on rapid publication of fundamental contributions to our understanding of microbiology. Its scope will reflect the immense range of fields within the microbial sciences, creating new opportunities for researchers to share findings that are transforming our understanding of human health and disease, ecosystems, neuroscience, agriculture, energy production, climate change, evolution, biogeochemical cycling, and food and drug production. Submissions will be encouraged of all high-quality work that makes fundamental contributions to our understanding of microbiology. mSphere™ will provide streamlined decisions, while carrying on ASM''s tradition for rigorous peer review.