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The occurrence of banana Fusarium wilt aggravates antibiotic resistance genes dissemination in soil
The spread of antibiotic resistance genes (ARGs) and subsequent soil-borne disease outbreaks are major threats to soil health and sustainable crop production. However, the relationship between occurrences of soil-borne diseases and the transmission of soil ARGs remains unclear. Here, soil ARGs, mobi...
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Published in: | Ecotoxicology and environmental safety 2024-09, Vol.283, p.116982, Article 116982 |
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description | The spread of antibiotic resistance genes (ARGs) and subsequent soil-borne disease outbreaks are major threats to soil health and sustainable crop production. However, the relationship between occurrences of soil-borne diseases and the transmission of soil ARGs remains unclear. Here, soil ARGs, mobile genetic elements and microbial communities from co-located disease suppressive and conducive banana orchards were deciphered using metagenomics and metatranscriptomics approaches. In total, 23 ARG types, with 399 subtypes, were detected using a metagenomics approach, whereas 23 ARG types, with 452 subtypes, were discovered using a metatranscriptomics method. Furthermore, the metagenomics analysis revealed that the ARG total abundance levels were greater in rhizospheres (0.45 ARGs/16S rRNA on average) compared with bulk (0.32 ARGs/16S rRNA on average) soils. Interestingly, metatranscriptomics revealed that the total ARG abundances were greater in disease-conducive (8.85 ARGs/16S rRNA on average) soils than disease suppressive (1.45 ARGs/16S rRNA on average) soils. Mobile genetic elements showed the same trends as ARGs. Network and binning analyses indicated that Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs. Furthermore, Bacillus was significantly and negatively correlated with Fusarium (P < 0.05, r = −0.84) and hosts of ARGs (i.e., Mycobacterium, Streptomyces, and Blastomonas). By comparing metagenomic and metatranscriptomic analyses,this study demonstrated that metatranscriptomics may be more sensitive in indicating ARGs activities in soil. Our findings enable the more accurate assessment of the transmission risk of ARGs. The data provide a new perspective for recognizing soil health, in which soil-borne disease outbreaks appear to be associated with ARG spread, whereas beneficial microbe enrichment may mitigate wilt disease and ARG transmission.
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•Soil-borne diseases and ARGs are strongly associated.•The total ARG abundances were greater in disease-conducive soils.•Mobile genetic elements showed the same trends as ARGs.•Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs.•Bacillus may contribute to reducing soil Fusarium and ARGs. |
doi_str_mv | 10.1016/j.ecoenv.2024.116982 |
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[Display omitted]
•Soil-borne diseases and ARGs are strongly associated.•The total ARG abundances were greater in disease-conducive soils.•Mobile genetic elements showed the same trends as ARGs.•Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs.•Bacillus may contribute to reducing soil Fusarium and ARGs.</description><identifier>ISSN: 0147-6513</identifier><identifier>ISSN: 1090-2414</identifier><identifier>EISSN: 1090-2414</identifier><identifier>DOI: 10.1016/j.ecoenv.2024.116982</identifier><identifier>PMID: 39217893</identifier><language>eng</language><publisher>Netherlands: Elsevier Inc</publisher><subject>Disease-suppressive soil ; Drug Resistance, Microbial - genetics ; Fusarium - genetics ; Metagenomics ; Musa - microbiology ; Plant Diseases - microbiology ; Resistance gene host ; RNA, Ribosomal, 16S - genetics ; Soil - chemistry ; Soil Microbiology ; Soil microbiome ; Soil resistome ; Soil-borne disease</subject><ispartof>Ecotoxicology and environmental safety, 2024-09, Vol.283, p.116982, Article 116982</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c353t-34955c42e22ae047c38f5429a7cb41488e258a5ab6e92320a232b8322b354fcd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0147651324010583$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3535,27903,27904,45759</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39217893$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Jiabao</creatorcontrib><creatorcontrib>Ou, Yannan</creatorcontrib><creatorcontrib>Li, Ruochen</creatorcontrib><creatorcontrib>Tao, Chengyuan</creatorcontrib><creatorcontrib>Liu, Hongjun</creatorcontrib><creatorcontrib>Li, Rong</creatorcontrib><creatorcontrib>Shen, Zongzhuan</creatorcontrib><creatorcontrib>Shen, Qirong</creatorcontrib><title>The occurrence of banana Fusarium wilt aggravates antibiotic resistance genes dissemination in soil</title><title>Ecotoxicology and environmental safety</title><addtitle>Ecotoxicol Environ Saf</addtitle><description>The spread of antibiotic resistance genes (ARGs) and subsequent soil-borne disease outbreaks are major threats to soil health and sustainable crop production. However, the relationship between occurrences of soil-borne diseases and the transmission of soil ARGs remains unclear. Here, soil ARGs, mobile genetic elements and microbial communities from co-located disease suppressive and conducive banana orchards were deciphered using metagenomics and metatranscriptomics approaches. In total, 23 ARG types, with 399 subtypes, were detected using a metagenomics approach, whereas 23 ARG types, with 452 subtypes, were discovered using a metatranscriptomics method. Furthermore, the metagenomics analysis revealed that the ARG total abundance levels were greater in rhizospheres (0.45 ARGs/16S rRNA on average) compared with bulk (0.32 ARGs/16S rRNA on average) soils. Interestingly, metatranscriptomics revealed that the total ARG abundances were greater in disease-conducive (8.85 ARGs/16S rRNA on average) soils than disease suppressive (1.45 ARGs/16S rRNA on average) soils. Mobile genetic elements showed the same trends as ARGs. Network and binning analyses indicated that Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs. Furthermore, Bacillus was significantly and negatively correlated with Fusarium (P < 0.05, r = −0.84) and hosts of ARGs (i.e., Mycobacterium, Streptomyces, and Blastomonas). By comparing metagenomic and metatranscriptomic analyses,this study demonstrated that metatranscriptomics may be more sensitive in indicating ARGs activities in soil. Our findings enable the more accurate assessment of the transmission risk of ARGs. The data provide a new perspective for recognizing soil health, in which soil-borne disease outbreaks appear to be associated with ARG spread, whereas beneficial microbe enrichment may mitigate wilt disease and ARG transmission.
[Display omitted]
•Soil-borne diseases and ARGs are strongly associated.•The total ARG abundances were greater in disease-conducive soils.•Mobile genetic elements showed the same trends as ARGs.•Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs.•Bacillus may contribute to reducing soil Fusarium and ARGs.</description><subject>Disease-suppressive soil</subject><subject>Drug Resistance, Microbial - genetics</subject><subject>Fusarium - genetics</subject><subject>Metagenomics</subject><subject>Musa - microbiology</subject><subject>Plant Diseases - microbiology</subject><subject>Resistance gene host</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Soil - chemistry</subject><subject>Soil Microbiology</subject><subject>Soil microbiome</subject><subject>Soil resistome</subject><subject>Soil-borne disease</subject><issn>0147-6513</issn><issn>1090-2414</issn><issn>1090-2414</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNp9kUtv3CAUhVHVqJk8_kFVedmNpzzHsKlURU0TKVI3yRpd48uUkW1SwFP135ep0ywrJEBwzrlcPkLeM7pllO0-HbboIs7HLadcbhnbGc3fkA2jhrZcMvmWbCiTXbtTTJyTi5wPlFJBlXpHzoXhrNNGbIh7_IFNdG5JCWdXt77pYa6juV0ypLBMza8wlgb2-wRHKJgbmEvoQyzBNQlzyAVOxj3O9W4IOeMUZighzk2YmxzDeEXOPIwZr1_WS_J0-_Xx5q59-P7t_ubLQ-uEEqUV0ijlJEfOAansnNBeSW6gc33tR2vkSoOCfoeGC06hTr0WnPdCSe8GcUnu19whwsE-pzBB-m0jBPv3IKa9hVSfPaL1nfQUUDPfCwl6AI01WjqpOw5eQc36uGY9p_hzwVzsFLLDcYQZ45KtoMZopQyjVSpXqUsx54T-tTSj9oTKHuyKyp5Q2RVVtX14qbD0Ew6vpn9squDzKsD6Z8eAyWYXTpCGkNCV2lT4f4U_WkmnRw</recordid><startdate>20240915</startdate><enddate>20240915</enddate><creator>Wang, Jiabao</creator><creator>Ou, Yannan</creator><creator>Li, Ruochen</creator><creator>Tao, Chengyuan</creator><creator>Liu, Hongjun</creator><creator>Li, Rong</creator><creator>Shen, Zongzhuan</creator><creator>Shen, Qirong</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>DOA</scope></search><sort><creationdate>20240915</creationdate><title>The occurrence of banana Fusarium wilt aggravates antibiotic resistance genes dissemination in soil</title><author>Wang, Jiabao ; Ou, Yannan ; Li, Ruochen ; Tao, Chengyuan ; Liu, Hongjun ; Li, Rong ; Shen, Zongzhuan ; Shen, Qirong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c353t-34955c42e22ae047c38f5429a7cb41488e258a5ab6e92320a232b8322b354fcd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Disease-suppressive soil</topic><topic>Drug Resistance, Microbial - genetics</topic><topic>Fusarium - genetics</topic><topic>Metagenomics</topic><topic>Musa - microbiology</topic><topic>Plant Diseases - microbiology</topic><topic>Resistance gene host</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Soil - chemistry</topic><topic>Soil Microbiology</topic><topic>Soil microbiome</topic><topic>Soil resistome</topic><topic>Soil-borne disease</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Jiabao</creatorcontrib><creatorcontrib>Ou, Yannan</creatorcontrib><creatorcontrib>Li, Ruochen</creatorcontrib><creatorcontrib>Tao, Chengyuan</creatorcontrib><creatorcontrib>Liu, Hongjun</creatorcontrib><creatorcontrib>Li, Rong</creatorcontrib><creatorcontrib>Shen, Zongzhuan</creatorcontrib><creatorcontrib>Shen, Qirong</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Ecotoxicology and environmental safety</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Jiabao</au><au>Ou, Yannan</au><au>Li, Ruochen</au><au>Tao, Chengyuan</au><au>Liu, Hongjun</au><au>Li, Rong</au><au>Shen, Zongzhuan</au><au>Shen, Qirong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The occurrence of banana Fusarium wilt aggravates antibiotic resistance genes dissemination in soil</atitle><jtitle>Ecotoxicology and environmental safety</jtitle><addtitle>Ecotoxicol Environ Saf</addtitle><date>2024-09-15</date><risdate>2024</risdate><volume>283</volume><spage>116982</spage><pages>116982-</pages><artnum>116982</artnum><issn>0147-6513</issn><issn>1090-2414</issn><eissn>1090-2414</eissn><abstract>The spread of antibiotic resistance genes (ARGs) and subsequent soil-borne disease outbreaks are major threats to soil health and sustainable crop production. However, the relationship between occurrences of soil-borne diseases and the transmission of soil ARGs remains unclear. Here, soil ARGs, mobile genetic elements and microbial communities from co-located disease suppressive and conducive banana orchards were deciphered using metagenomics and metatranscriptomics approaches. In total, 23 ARG types, with 399 subtypes, were detected using a metagenomics approach, whereas 23 ARG types, with 452 subtypes, were discovered using a metatranscriptomics method. Furthermore, the metagenomics analysis revealed that the ARG total abundance levels were greater in rhizospheres (0.45 ARGs/16S rRNA on average) compared with bulk (0.32 ARGs/16S rRNA on average) soils. Interestingly, metatranscriptomics revealed that the total ARG abundances were greater in disease-conducive (8.85 ARGs/16S rRNA on average) soils than disease suppressive (1.45 ARGs/16S rRNA on average) soils. Mobile genetic elements showed the same trends as ARGs. Network and binning analyses indicated that Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs. Furthermore, Bacillus was significantly and negatively correlated with Fusarium (P < 0.05, r = −0.84) and hosts of ARGs (i.e., Mycobacterium, Streptomyces, and Blastomonas). By comparing metagenomic and metatranscriptomic analyses,this study demonstrated that metatranscriptomics may be more sensitive in indicating ARGs activities in soil. Our findings enable the more accurate assessment of the transmission risk of ARGs. The data provide a new perspective for recognizing soil health, in which soil-borne disease outbreaks appear to be associated with ARG spread, whereas beneficial microbe enrichment may mitigate wilt disease and ARG transmission.
[Display omitted]
•Soil-borne diseases and ARGs are strongly associated.•The total ARG abundances were greater in disease-conducive soils.•Mobile genetic elements showed the same trends as ARGs.•Mycobacterium, Streptomyces, and Blastomonas are the main potential hosts of ARGs.•Bacillus may contribute to reducing soil Fusarium and ARGs.</abstract><cop>Netherlands</cop><pub>Elsevier Inc</pub><pmid>39217893</pmid><doi>10.1016/j.ecoenv.2024.116982</doi><oa>free_for_read</oa></addata></record> |
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subjects | Disease-suppressive soil Drug Resistance, Microbial - genetics Fusarium - genetics Metagenomics Musa - microbiology Plant Diseases - microbiology Resistance gene host RNA, Ribosomal, 16S - genetics Soil - chemistry Soil Microbiology Soil microbiome Soil resistome Soil-borne disease |
title | The occurrence of banana Fusarium wilt aggravates antibiotic resistance genes dissemination in soil |
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