Increased antibiotic resistance gene abundance linked to intensive bacterial competition in the phyllosphere across an elevational gradient
Antibiotic resistance genes (ARGs) are ancient and widespread in natural habitats, providing survival advantages for microbiomes under challenging conditions. In mountain ecosystems, phyllosphere bacterial communities face multiple stress conditions, and the elevational gradients of mountains repres...
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description | Antibiotic resistance genes (ARGs) are ancient and widespread in natural habitats, providing survival advantages for microbiomes under challenging conditions. In mountain ecosystems, phyllosphere bacterial communities face multiple stress conditions, and the elevational gradients of mountains represent crucial environmental gradients for studying biodiversity distribution patterns. However, the distribution patterns of ARGs in the phyllosphere along elevational gradients, and their correlation with bacterial community structures, remain poorly understood. Here, we applied metagenomic analyses to investigate the abundance and diversity of ARGs in 88 phyllosphere samples collected from Mount Tianmu, a national natural reserve. Our results showed that the abundance of ARGs in the phyllosphere increased along elevational gradients and was dominated by multidrug resistance and efflux pumps. The composition of bacterial communities, rather than plant traits or abiotic factors, significantly affected ARG abundance. Moreover, increased ARG abundance was correlated with greater phylogenetic overdispersion and a greater proportion of negative associations in the bacterial co‐occurrence networks, suggesting that bacterial competition primarily shapes phyllosphere resistomes. These findings constitute a major advance in the biodiversity of phyllosphere resistomes along elevations, emphasizing the significant impact of bacterial community structure and assembly on ARG distribution, and are essential for understanding the emergence of ARGs.
Minimal research has been conducted on the phyllosphere resistome in relatively pristine environments. This study reports an increase in the abundance of phyllosphere resistomes along an elevational gradient in a national natural reserve, with implications for the spread of antibiotic resistance genes (ARGs). |
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Minimal research has been conducted on the phyllosphere resistome in relatively pristine environments. This study reports an increase in the abundance of phyllosphere resistomes along an elevational gradient in a national natural reserve, with implications for the spread of antibiotic resistance genes (ARGs).</description><identifier>ISSN: 1758-2229</identifier><identifier>EISSN: 1758-2229</identifier><identifier>DOI: 10.1111/1758-2229.70042</identifier><identifier>PMID: 39572861</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Altitude ; Anti-Bacterial Agents - pharmacology ; Bacteria - classification ; Bacteria - genetics ; Bacteria - isolation & purification ; Biodiversity ; Drug Resistance, Bacterial - genetics ; Ecosystem ; Genes, Bacterial - genetics ; Metagenomics ; Microbiota - genetics ; Phylogeny</subject><ispartof>Environmental microbiology reports, 2024-12, Vol.16 (6), p.e70042-n/a</ispartof><rights>2024 The Author(s). published by John Wiley & Sons Ltd.</rights><rights>2024 The Author(s). Environmental Microbiology Reports published by John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c2692-b029728b49ed37de482e33ceb60622c9bf4b22a7ce86c893bc5474df33e163a03</cites><orcidid>0000-0002-1730-3433 ; 0000-0001-6701-5790</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1758-2229.70042$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1758-2229.70042$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,11541,27901,27902,45550,45551,46027,46451</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39572861$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ding, Yihui</creatorcontrib><creatorcontrib>Ma, Rui‐Ao</creatorcontrib><creatorcontrib>Zhang, Ran</creatorcontrib><creatorcontrib>Zhang, Hongwei</creatorcontrib><creatorcontrib>Zhang, Jian</creatorcontrib><creatorcontrib>Li, Shaopeng</creatorcontrib><creatorcontrib>Zhang, Si‐Yu</creatorcontrib><title>Increased antibiotic resistance gene abundance linked to intensive bacterial competition in the phyllosphere across an elevational gradient</title><title>Environmental microbiology reports</title><addtitle>Environ Microbiol Rep</addtitle><description>Antibiotic resistance genes (ARGs) are ancient and widespread in natural habitats, providing survival advantages for microbiomes under challenging conditions. In mountain ecosystems, phyllosphere bacterial communities face multiple stress conditions, and the elevational gradients of mountains represent crucial environmental gradients for studying biodiversity distribution patterns. However, the distribution patterns of ARGs in the phyllosphere along elevational gradients, and their correlation with bacterial community structures, remain poorly understood. Here, we applied metagenomic analyses to investigate the abundance and diversity of ARGs in 88 phyllosphere samples collected from Mount Tianmu, a national natural reserve. Our results showed that the abundance of ARGs in the phyllosphere increased along elevational gradients and was dominated by multidrug resistance and efflux pumps. The composition of bacterial communities, rather than plant traits or abiotic factors, significantly affected ARG abundance. Moreover, increased ARG abundance was correlated with greater phylogenetic overdispersion and a greater proportion of negative associations in the bacterial co‐occurrence networks, suggesting that bacterial competition primarily shapes phyllosphere resistomes. These findings constitute a major advance in the biodiversity of phyllosphere resistomes along elevations, emphasizing the significant impact of bacterial community structure and assembly on ARG distribution, and are essential for understanding the emergence of ARGs.
Minimal research has been conducted on the phyllosphere resistome in relatively pristine environments. This study reports an increase in the abundance of phyllosphere resistomes along an elevational gradient in a national natural reserve, with implications for the spread of antibiotic resistance genes (ARGs).</description><subject>Altitude</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Biodiversity</subject><subject>Drug Resistance, Bacterial - genetics</subject><subject>Ecosystem</subject><subject>Genes, Bacterial - genetics</subject><subject>Metagenomics</subject><subject>Microbiota - genetics</subject><subject>Phylogeny</subject><issn>1758-2229</issn><issn>1758-2229</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqFkU1PAjEQhhujEUTP3kyPXoBuu-zH0RBUEo0XPTdtdxaqpbu2BcNv8E9bWCTe7GU6nWfeTt5B6DohoySecZJPiiGltBzlhKT0BPWPL6d_7j104f07IVlaEnqOeqyc5LTIkj76nlvlQHiosLBBS90ErbADr30QVgFegAUs5NpW-9Ro-xHZ0GBtA1ivN4ClUAGcFgarZtVC0EE3NtZxWAJul1tjGt8uwUUd5Rrv408YDGzEjotdCycqDTZcorNaGA9XhzhAb_ez1-nj8OnlYT69exoqmpV0KAkt4_QyLaFieQVpQYExBTIjGaWqlHUqKRW5giJTRcmkmqR5WtWMQZIxQdgA3Xa6rWs-1-ADX2mvwBhhoVl7zhKWFBOS5zSi4w7dD-6g5q3TK-G2PCF8twG-85jvPOb7DcSOm4P4Wq6gOvK_lkcg64AvbWD7nx6fPc_TTvkHa1STlw</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Ding, Yihui</creator><creator>Ma, Rui‐Ao</creator><creator>Zhang, Ran</creator><creator>Zhang, Hongwei</creator><creator>Zhang, Jian</creator><creator>Li, Shaopeng</creator><creator>Zhang, Si‐Yu</creator><general>John Wiley & Sons, Inc</general><scope>24P</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><orcidid>https://orcid.org/0000-0002-1730-3433</orcidid><orcidid>https://orcid.org/0000-0001-6701-5790</orcidid></search><sort><creationdate>202412</creationdate><title>Increased antibiotic resistance gene abundance linked to intensive bacterial competition in the phyllosphere across an elevational gradient</title><author>Ding, Yihui ; Ma, Rui‐Ao ; Zhang, Ran ; Zhang, Hongwei ; Zhang, Jian ; Li, Shaopeng ; Zhang, Si‐Yu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c2692-b029728b49ed37de482e33ceb60622c9bf4b22a7ce86c893bc5474df33e163a03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Altitude</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Bacteria - classification</topic><topic>Bacteria - genetics</topic><topic>Bacteria - isolation & purification</topic><topic>Biodiversity</topic><topic>Drug Resistance, Bacterial - genetics</topic><topic>Ecosystem</topic><topic>Genes, Bacterial - genetics</topic><topic>Metagenomics</topic><topic>Microbiota - genetics</topic><topic>Phylogeny</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ding, Yihui</creatorcontrib><creatorcontrib>Ma, Rui‐Ao</creatorcontrib><creatorcontrib>Zhang, Ran</creatorcontrib><creatorcontrib>Zhang, Hongwei</creatorcontrib><creatorcontrib>Zhang, Jian</creatorcontrib><creatorcontrib>Li, Shaopeng</creatorcontrib><creatorcontrib>Zhang, Si‐Yu</creatorcontrib><collection>Wiley Online Library 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><jtitle>Environmental microbiology reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ding, Yihui</au><au>Ma, Rui‐Ao</au><au>Zhang, Ran</au><au>Zhang, Hongwei</au><au>Zhang, Jian</au><au>Li, Shaopeng</au><au>Zhang, Si‐Yu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Increased antibiotic resistance gene abundance linked to intensive bacterial competition in the phyllosphere across an elevational gradient</atitle><jtitle>Environmental microbiology reports</jtitle><addtitle>Environ Microbiol Rep</addtitle><date>2024-12</date><risdate>2024</risdate><volume>16</volume><issue>6</issue><spage>e70042</spage><epage>n/a</epage><pages>e70042-n/a</pages><issn>1758-2229</issn><eissn>1758-2229</eissn><abstract>Antibiotic resistance genes (ARGs) are ancient and widespread in natural habitats, providing survival advantages for microbiomes under challenging conditions. In mountain ecosystems, phyllosphere bacterial communities face multiple stress conditions, and the elevational gradients of mountains represent crucial environmental gradients for studying biodiversity distribution patterns. However, the distribution patterns of ARGs in the phyllosphere along elevational gradients, and their correlation with bacterial community structures, remain poorly understood. Here, we applied metagenomic analyses to investigate the abundance and diversity of ARGs in 88 phyllosphere samples collected from Mount Tianmu, a national natural reserve. Our results showed that the abundance of ARGs in the phyllosphere increased along elevational gradients and was dominated by multidrug resistance and efflux pumps. The composition of bacterial communities, rather than plant traits or abiotic factors, significantly affected ARG abundance. Moreover, increased ARG abundance was correlated with greater phylogenetic overdispersion and a greater proportion of negative associations in the bacterial co‐occurrence networks, suggesting that bacterial competition primarily shapes phyllosphere resistomes. These findings constitute a major advance in the biodiversity of phyllosphere resistomes along elevations, emphasizing the significant impact of bacterial community structure and assembly on ARG distribution, and are essential for understanding the emergence of ARGs.
Minimal research has been conducted on the phyllosphere resistome in relatively pristine environments. This study reports an increase in the abundance of phyllosphere resistomes along an elevational gradient in a national natural reserve, with implications for the spread of antibiotic resistance genes (ARGs).</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>39572861</pmid><doi>10.1111/1758-2229.70042</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-1730-3433</orcidid><orcidid>https://orcid.org/0000-0001-6701-5790</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Altitude Anti-Bacterial Agents - pharmacology Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Biodiversity Drug Resistance, Bacterial - genetics Ecosystem Genes, Bacterial - genetics Metagenomics Microbiota - genetics Phylogeny |
title | Increased antibiotic resistance gene abundance linked to intensive bacterial competition in the phyllosphere across an elevational gradient |
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