Diverse bacterial hosts and potential risk of antibiotic resistomes in ship ballast water revealed by metagenomic binning
Ship ballast water promoting the long-range migration of antibiotic resistance genes (ARGs) has raised a great concern. This study attempted to reveal ARGs profile in ballast water and decipher their hosts and potential risk using metagenomic approaches. In total, 710 subtypes across 26 ARG types we...
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description | Ship ballast water promoting the long-range migration of antibiotic resistance genes (ARGs) has raised a great concern. This study attempted to reveal ARGs profile in ballast water and decipher their hosts and potential risk using metagenomic approaches. In total, 710 subtypes across 26 ARG types were identified among the ballast water samples from 13 ships of 11 countries and regions, and multidrug resistance genes were the most dominant ARGs. The composition of ARGs were obviously different across samples, and only 5% of the ARG subtypes were shared by all samples. Procrustes analysis showed the bacterial community contributed more than the mobile genetic elements (MGEs) in shaping the antibiotic resistome. Further, 79 metagenome-assembled genomes (46 genera belong to four phyla) were identified as ARG hosts, with predominantly affiliated with the Proteobacteria. Notably, potential human pathogens (Alcaligenes, Mycolicibacterium, Rhodococcus and Pseudomonas) were also recognized as the ARG hosts. Above 30% of the ARGs hosts contained the MGEs simultaneously, supporting a pronounced horizontal gene transfer capability. A total of 43 subtypes (six percent of overall ARGs) of ARGs were assessed with high-risk, of which 23 subtypes belonged to risk Rank I (including rsmA, ugd, etc.) and 20 subtypes to the risk Rank II (including aac(6)-I, sul1, etc.). In addition, antibiotic resistance risk index indicated the risk of ARGs in ballast water from choke points of maritime trade routes was significantly higher than that from other regions. Overall, this study offers insights for risk evaluation and management of antibiotic resistance in ballast water.
[Display omitted]
•710 subtypes (26 types) ARGs were detected in ballast water by metagenomic analysis.•Bacterial community was the premier driver of ARGs in ballast water.•Pathogenic and multi-drug resistant bacteria were found in ballast water.•Ballast water from choke points of maritime trade routes show higher risk of ARGs. |
doi_str_mv | 10.1016/j.envres.2024.119056 |
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[Display omitted]
•710 subtypes (26 types) ARGs were detected in ballast water by metagenomic analysis.•Bacterial community was the premier driver of ARGs in ballast water.•Pathogenic and multi-drug resistant bacteria were found in ballast water.•Ballast water from choke points of maritime trade routes show higher risk of ARGs.</description><identifier>ISSN: 0013-9351</identifier><identifier>ISSN: 1096-0953</identifier><identifier>EISSN: 1096-0953</identifier><identifier>DOI: 10.1016/j.envres.2024.119056</identifier><identifier>PMID: 38704005</identifier><language>eng</language><publisher>Netherlands: Elsevier Inc</publisher><subject>Alcaligenes ; antibiotic resistance ; Antibiotic resistance genes ; antibiotics ; bacterial communities ; Bacterial host ; ballast water ; Horizontal gene transfer ; humans ; Long distance migration ; metagenomics ; multiple drug resistance ; Pseudomonas ; risk ; Risk assessment ; Ship ballast water ; trade</subject><ispartof>Environmental research, 2024-07, Vol.253, p.119056, Article 119056</ispartof><rights>2024 Elsevier Inc.</rights><rights>Copyright © 2024. Published by Elsevier Inc.</rights><rights>Copyright © 2024 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c344t-cc4b85606cf599a5bb3c704c48f5bc91c2bab39ab229dc1e225d14a0fd11e443</cites><orcidid>0000-0003-1267-7396</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0013935124009605$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38704005$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lv, Baoyi</creatorcontrib><creatorcontrib>Jiang, Changhai</creatorcontrib><creatorcontrib>Han, Yangchun</creatorcontrib><creatorcontrib>Wu, Dong</creatorcontrib><creatorcontrib>Jin, Ling</creatorcontrib><creatorcontrib>Zhu, Guorong</creatorcontrib><creatorcontrib>An, Tingxuan</creatorcontrib><creatorcontrib>Shi, Jianhong</creatorcontrib><title>Diverse bacterial hosts and potential risk of antibiotic resistomes in ship ballast water revealed by metagenomic binning</title><title>Environmental research</title><addtitle>Environ Res</addtitle><description>Ship ballast water promoting the long-range migration of antibiotic resistance genes (ARGs) has raised a great concern. This study attempted to reveal ARGs profile in ballast water and decipher their hosts and potential risk using metagenomic approaches. In total, 710 subtypes across 26 ARG types were identified among the ballast water samples from 13 ships of 11 countries and regions, and multidrug resistance genes were the most dominant ARGs. The composition of ARGs were obviously different across samples, and only 5% of the ARG subtypes were shared by all samples. Procrustes analysis showed the bacterial community contributed more than the mobile genetic elements (MGEs) in shaping the antibiotic resistome. Further, 79 metagenome-assembled genomes (46 genera belong to four phyla) were identified as ARG hosts, with predominantly affiliated with the Proteobacteria. Notably, potential human pathogens (Alcaligenes, Mycolicibacterium, Rhodococcus and Pseudomonas) were also recognized as the ARG hosts. Above 30% of the ARGs hosts contained the MGEs simultaneously, supporting a pronounced horizontal gene transfer capability. A total of 43 subtypes (six percent of overall ARGs) of ARGs were assessed with high-risk, of which 23 subtypes belonged to risk Rank I (including rsmA, ugd, etc.) and 20 subtypes to the risk Rank II (including aac(6)-I, sul1, etc.). In addition, antibiotic resistance risk index indicated the risk of ARGs in ballast water from choke points of maritime trade routes was significantly higher than that from other regions. Overall, this study offers insights for risk evaluation and management of antibiotic resistance in ballast water.
[Display omitted]
•710 subtypes (26 types) ARGs were detected in ballast water by metagenomic analysis.•Bacterial community was the premier driver of ARGs in ballast water.•Pathogenic and multi-drug resistant bacteria were found in ballast water.•Ballast water from choke points of maritime trade routes show higher risk of ARGs.</description><subject>Alcaligenes</subject><subject>antibiotic resistance</subject><subject>Antibiotic resistance genes</subject><subject>antibiotics</subject><subject>bacterial communities</subject><subject>Bacterial host</subject><subject>ballast water</subject><subject>Horizontal gene transfer</subject><subject>humans</subject><subject>Long distance migration</subject><subject>metagenomics</subject><subject>multiple drug resistance</subject><subject>Pseudomonas</subject><subject>risk</subject><subject>Risk assessment</subject><subject>Ship ballast water</subject><subject>trade</subject><issn>0013-9351</issn><issn>1096-0953</issn><issn>1096-0953</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkU9v3CAQxVHVqtmk_QZVxDEXbwcDjrlUitK_0kq95I4AjxM2NmyB3Wi_fVk5zTE9IUa_995oHiGfGKwZsO7zdo3hkDCvW2jFmjEFsntDVgxU14CS_C1ZATDeKC7ZGTnPeVu_THJ4T854fw0CQK7I8as_YMpIrXEFkzcTfYi5ZGrCQHexYCinWfL5kcaxTou3PhbvaI32ucQZM_WB5ge_qx7TZHKhT6ZaVeCAZsKB2iOdsZh7DHGuQutD8OH-A3k3minjx-f3gtx9_3Z3-7PZ_P7x6_Zm0zguRGmcE7aXHXRulEoZaS13dXkn-lFap5hrrbFcGdu2anAM21YOTBgYB8ZQCH5BrhbbXYp_9piLnn12WBcNGPdZ83qS6571Lfs_ChKUgE5CRcWCuhRzTjjqXfKzSUfNQJ_q0Vu91KNP9eilniq7fE7Y2xmHF9G_PirwZQGwXuTgMensPAaHg0_oih6ifz3hL2WupQM</recordid><startdate>20240715</startdate><enddate>20240715</enddate><creator>Lv, Baoyi</creator><creator>Jiang, Changhai</creator><creator>Han, Yangchun</creator><creator>Wu, Dong</creator><creator>Jin, Ling</creator><creator>Zhu, Guorong</creator><creator>An, Tingxuan</creator><creator>Shi, Jianhong</creator><general>Elsevier Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-1267-7396</orcidid></search><sort><creationdate>20240715</creationdate><title>Diverse bacterial hosts and potential risk of antibiotic resistomes in ship ballast water revealed by metagenomic binning</title><author>Lv, Baoyi ; Jiang, Changhai ; Han, Yangchun ; Wu, Dong ; Jin, Ling ; Zhu, Guorong ; An, Tingxuan ; Shi, Jianhong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c344t-cc4b85606cf599a5bb3c704c48f5bc91c2bab39ab229dc1e225d14a0fd11e443</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Alcaligenes</topic><topic>antibiotic resistance</topic><topic>Antibiotic resistance genes</topic><topic>antibiotics</topic><topic>bacterial communities</topic><topic>Bacterial host</topic><topic>ballast water</topic><topic>Horizontal gene transfer</topic><topic>humans</topic><topic>Long distance migration</topic><topic>metagenomics</topic><topic>multiple drug resistance</topic><topic>Pseudomonas</topic><topic>risk</topic><topic>Risk assessment</topic><topic>Ship ballast water</topic><topic>trade</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lv, Baoyi</creatorcontrib><creatorcontrib>Jiang, Changhai</creatorcontrib><creatorcontrib>Han, Yangchun</creatorcontrib><creatorcontrib>Wu, Dong</creatorcontrib><creatorcontrib>Jin, Ling</creatorcontrib><creatorcontrib>Zhu, Guorong</creatorcontrib><creatorcontrib>An, Tingxuan</creatorcontrib><creatorcontrib>Shi, Jianhong</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Environmental research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lv, Baoyi</au><au>Jiang, Changhai</au><au>Han, Yangchun</au><au>Wu, Dong</au><au>Jin, Ling</au><au>Zhu, Guorong</au><au>An, Tingxuan</au><au>Shi, Jianhong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diverse bacterial hosts and potential risk of antibiotic resistomes in ship ballast water revealed by metagenomic binning</atitle><jtitle>Environmental research</jtitle><addtitle>Environ Res</addtitle><date>2024-07-15</date><risdate>2024</risdate><volume>253</volume><spage>119056</spage><pages>119056-</pages><artnum>119056</artnum><issn>0013-9351</issn><issn>1096-0953</issn><eissn>1096-0953</eissn><abstract>Ship ballast water promoting the long-range migration of antibiotic resistance genes (ARGs) has raised a great concern. This study attempted to reveal ARGs profile in ballast water and decipher their hosts and potential risk using metagenomic approaches. In total, 710 subtypes across 26 ARG types were identified among the ballast water samples from 13 ships of 11 countries and regions, and multidrug resistance genes were the most dominant ARGs. The composition of ARGs were obviously different across samples, and only 5% of the ARG subtypes were shared by all samples. Procrustes analysis showed the bacterial community contributed more than the mobile genetic elements (MGEs) in shaping the antibiotic resistome. Further, 79 metagenome-assembled genomes (46 genera belong to four phyla) were identified as ARG hosts, with predominantly affiliated with the Proteobacteria. Notably, potential human pathogens (Alcaligenes, Mycolicibacterium, Rhodococcus and Pseudomonas) were also recognized as the ARG hosts. Above 30% of the ARGs hosts contained the MGEs simultaneously, supporting a pronounced horizontal gene transfer capability. A total of 43 subtypes (six percent of overall ARGs) of ARGs were assessed with high-risk, of which 23 subtypes belonged to risk Rank I (including rsmA, ugd, etc.) and 20 subtypes to the risk Rank II (including aac(6)-I, sul1, etc.). In addition, antibiotic resistance risk index indicated the risk of ARGs in ballast water from choke points of maritime trade routes was significantly higher than that from other regions. Overall, this study offers insights for risk evaluation and management of antibiotic resistance in ballast water.
[Display omitted]
•710 subtypes (26 types) ARGs were detected in ballast water by metagenomic analysis.•Bacterial community was the premier driver of ARGs in ballast water.•Pathogenic and multi-drug resistant bacteria were found in ballast water.•Ballast water from choke points of maritime trade routes show higher risk of ARGs.</abstract><cop>Netherlands</cop><pub>Elsevier Inc</pub><pmid>38704005</pmid><doi>10.1016/j.envres.2024.119056</doi><orcidid>https://orcid.org/0000-0003-1267-7396</orcidid></addata></record> |
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subjects | Alcaligenes antibiotic resistance Antibiotic resistance genes antibiotics bacterial communities Bacterial host ballast water Horizontal gene transfer humans Long distance migration metagenomics multiple drug resistance Pseudomonas risk Risk assessment Ship ballast water trade |
title | Diverse bacterial hosts and potential risk of antibiotic resistomes in ship ballast water revealed by metagenomic binning |
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