Core Microbiota in the Rhizosphere of Heavy Metal Accumulators and Its Contribution to Plant Performance
Persistent microbial symbioses can confer greater fitness to their host under unfavorable conditions, but manipulating such beneficial interactions necessitates a mechanistic understanding of the consistently important microbiomes for the plant. Here, we examined the phylogenetic profiles and plant-...
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Veröffentlicht in: | Environmental science & technology 2022-09, Vol.56 (18), p.12975-12987 |
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creator | Luo, Jipeng Gu, Shaohua Guo, Xinyu Liu, Yuankun Tao, Qi Zhao, He-Ping Liang, Yongchao Banerjee, Samiran Li, Tingqiang |
description | Persistent microbial symbioses can confer greater fitness to their host under unfavorable conditions, but manipulating such beneficial interactions necessitates a mechanistic understanding of the consistently important microbiomes for the plant. Here, we examined the phylogenetic profiles and plant-beneficial traits of the core microbiota that consistently inhabits the rhizosphere of four divergent Cd hyperaccumulators and an accumulator. We evidenced the existence of a conserved core rhizosphere microbiota in each plant distinct from that in the non-hyperaccumulating plant. Members of Burkholderiaceae and Sphingomonas were the shared cores across hyperaccumulators and accumulators. Several keystone taxa in the rhizosphere networks were part of the core microbiota, the abundance of which was an important predictor of plant Cd accumulation. Furthermore, an inoculation experiment with synthetic communities comprising isolates belonging to the shared cores indicated that core microorganisms could facilitate plant growth and metal tolerance. Using RNA-based stable isotope probing, we discovered that abundant core taxa overlapped with active rhizobacteria utilizing root exudates, implying that the core rhizosphere microbiota assimilating plant-derived carbon may provide benefits to plant growth and host phenotype such as Cd accumulation. Our study suggests common principles underpinning hyperaccumulator–microbiome interactions, where plants consistently interact with a core set of microbes contributing to host fitness and plant performance. These findings lay the foundation for harnessing the persistent root microbiomes to accelerate the restoration of metal-disturbed soils. |
doi_str_mv | 10.1021/acs.est.1c08832 |
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Here, we examined the phylogenetic profiles and plant-beneficial traits of the core microbiota that consistently inhabits the rhizosphere of four divergent Cd hyperaccumulators and an accumulator. We evidenced the existence of a conserved core rhizosphere microbiota in each plant distinct from that in the non-hyperaccumulating plant. Members of Burkholderiaceae and Sphingomonas were the shared cores across hyperaccumulators and accumulators. Several keystone taxa in the rhizosphere networks were part of the core microbiota, the abundance of which was an important predictor of plant Cd accumulation. Furthermore, an inoculation experiment with synthetic communities comprising isolates belonging to the shared cores indicated that core microorganisms could facilitate plant growth and metal tolerance. Using RNA-based stable isotope probing, we discovered that abundant core taxa overlapped with active rhizobacteria utilizing root exudates, implying that the core rhizosphere microbiota assimilating plant-derived carbon may provide benefits to plant growth and host phenotype such as Cd accumulation. Our study suggests common principles underpinning hyperaccumulator–microbiome interactions, where plants consistently interact with a core set of microbes contributing to host fitness and plant performance. These findings lay the foundation for harnessing the persistent root microbiomes to accelerate the restoration of metal-disturbed soils.</description><identifier>ISSN: 0013-936X</identifier><identifier>EISSN: 1520-5851</identifier><identifier>DOI: 10.1021/acs.est.1c08832</identifier><language>eng</language><publisher>Easton: American Chemical Society</publisher><subject>Accumulation ; Accumulators ; Cadmium ; Contaminants in Aquatic and Terrestrial Environments ; Cores ; Exudates ; Exudation ; Fitness ; Heavy metals ; Host plants ; Inoculation ; Microbiomes ; Microbiota ; Microorganisms ; Phenotypes ; Phylogeny ; Plant growth ; Plants ; Rhizosphere ; Stable isotopes ; Symbiosis</subject><ispartof>Environmental science & technology, 2022-09, Vol.56 (18), p.12975-12987</ispartof><rights>2022 American Chemical Society</rights><rights>Copyright American Chemical Society Sep 20, 2022</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a268t-4b5ccf2797f2e89863adfa212d8c6a1f6d7abbf18549aa6e64939892c5d778843</citedby><cites>FETCH-LOGICAL-a268t-4b5ccf2797f2e89863adfa212d8c6a1f6d7abbf18549aa6e64939892c5d778843</cites><orcidid>0000-0002-5177-8010 ; 0000-0003-4448-4871</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.est.1c08832$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.est.1c08832$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,776,780,2752,27053,27901,27902,56713,56763</link.rule.ids></links><search><creatorcontrib>Luo, Jipeng</creatorcontrib><creatorcontrib>Gu, Shaohua</creatorcontrib><creatorcontrib>Guo, Xinyu</creatorcontrib><creatorcontrib>Liu, Yuankun</creatorcontrib><creatorcontrib>Tao, Qi</creatorcontrib><creatorcontrib>Zhao, He-Ping</creatorcontrib><creatorcontrib>Liang, Yongchao</creatorcontrib><creatorcontrib>Banerjee, Samiran</creatorcontrib><creatorcontrib>Li, Tingqiang</creatorcontrib><title>Core Microbiota in the Rhizosphere of Heavy Metal Accumulators and Its Contribution to Plant Performance</title><title>Environmental science & technology</title><addtitle>Environ. Sci. Technol</addtitle><description>Persistent microbial symbioses can confer greater fitness to their host under unfavorable conditions, but manipulating such beneficial interactions necessitates a mechanistic understanding of the consistently important microbiomes for the plant. Here, we examined the phylogenetic profiles and plant-beneficial traits of the core microbiota that consistently inhabits the rhizosphere of four divergent Cd hyperaccumulators and an accumulator. We evidenced the existence of a conserved core rhizosphere microbiota in each plant distinct from that in the non-hyperaccumulating plant. Members of Burkholderiaceae and Sphingomonas were the shared cores across hyperaccumulators and accumulators. Several keystone taxa in the rhizosphere networks were part of the core microbiota, the abundance of which was an important predictor of plant Cd accumulation. Furthermore, an inoculation experiment with synthetic communities comprising isolates belonging to the shared cores indicated that core microorganisms could facilitate plant growth and metal tolerance. Using RNA-based stable isotope probing, we discovered that abundant core taxa overlapped with active rhizobacteria utilizing root exudates, implying that the core rhizosphere microbiota assimilating plant-derived carbon may provide benefits to plant growth and host phenotype such as Cd accumulation. Our study suggests common principles underpinning hyperaccumulator–microbiome interactions, where plants consistently interact with a core set of microbes contributing to host fitness and plant performance. These findings lay the foundation for harnessing the persistent root microbiomes to accelerate the restoration of metal-disturbed soils.</description><subject>Accumulation</subject><subject>Accumulators</subject><subject>Cadmium</subject><subject>Contaminants in Aquatic and Terrestrial Environments</subject><subject>Cores</subject><subject>Exudates</subject><subject>Exudation</subject><subject>Fitness</subject><subject>Heavy metals</subject><subject>Host plants</subject><subject>Inoculation</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microorganisms</subject><subject>Phenotypes</subject><subject>Phylogeny</subject><subject>Plant growth</subject><subject>Plants</subject><subject>Rhizosphere</subject><subject>Stable isotopes</subject><subject>Symbiosis</subject><issn>0013-936X</issn><issn>1520-5851</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp1kMFLwzAUh4MoOKdnrwEvgnRL0jZNj2OoG2w4RMFbeU0T2tE1M0mF-debsuFB8PQO7_v9eO9D6JaSCSWMTkG6iXJ-QiURImZnaERTRqJUpPQcjQihcZTH_OMSXTm3JYSwmIgRqufGKrxupDVlYzzgpsO-Vvi1br6N29cqbI3GCwVfB7xWHlo8k7Lf9S14Yx2GrsJL7_DcdN42Ze8bEwoM3rTQebxRVhu7g06qa3ShoXXq5jTH6P3p8W2-iFYvz8v5bBUB48JHSZlKqVmWZ5opkQseQ6WBUVYJyYFqXmVQlpqKNMkBuOJJHuciZzKtskyIJB6j-2Pv3prPPggpdo2Tqg33KNO7gmWUhs8TPqB3f9Ct6W0XrhsongrOExao6ZEKipyzShd72-zAHgpKisF8EcwXQ_pkPiQejolh8Vv5H_0DrmSGzQ</recordid><startdate>20220920</startdate><enddate>20220920</enddate><creator>Luo, Jipeng</creator><creator>Gu, Shaohua</creator><creator>Guo, Xinyu</creator><creator>Liu, Yuankun</creator><creator>Tao, Qi</creator><creator>Zhao, He-Ping</creator><creator>Liang, Yongchao</creator><creator>Banerjee, Samiran</creator><creator>Li, Tingqiang</creator><general>American Chemical Society</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7ST</scope><scope>7T7</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-5177-8010</orcidid><orcidid>https://orcid.org/0000-0003-4448-4871</orcidid></search><sort><creationdate>20220920</creationdate><title>Core Microbiota in the Rhizosphere of Heavy Metal Accumulators and Its Contribution to Plant Performance</title><author>Luo, Jipeng ; Gu, Shaohua ; Guo, Xinyu ; Liu, Yuankun ; Tao, Qi ; Zhao, He-Ping ; Liang, Yongchao ; Banerjee, Samiran ; Li, Tingqiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a268t-4b5ccf2797f2e89863adfa212d8c6a1f6d7abbf18549aa6e64939892c5d778843</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Accumulation</topic><topic>Accumulators</topic><topic>Cadmium</topic><topic>Contaminants in Aquatic and Terrestrial Environments</topic><topic>Cores</topic><topic>Exudates</topic><topic>Exudation</topic><topic>Fitness</topic><topic>Heavy metals</topic><topic>Host plants</topic><topic>Inoculation</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Microorganisms</topic><topic>Phenotypes</topic><topic>Phylogeny</topic><topic>Plant growth</topic><topic>Plants</topic><topic>Rhizosphere</topic><topic>Stable isotopes</topic><topic>Symbiosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Luo, Jipeng</creatorcontrib><creatorcontrib>Gu, Shaohua</creatorcontrib><creatorcontrib>Guo, Xinyu</creatorcontrib><creatorcontrib>Liu, Yuankun</creatorcontrib><creatorcontrib>Tao, Qi</creatorcontrib><creatorcontrib>Zhao, He-Ping</creatorcontrib><creatorcontrib>Liang, Yongchao</creatorcontrib><creatorcontrib>Banerjee, Samiran</creatorcontrib><creatorcontrib>Li, Tingqiang</creatorcontrib><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental science & technology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Luo, Jipeng</au><au>Gu, Shaohua</au><au>Guo, Xinyu</au><au>Liu, Yuankun</au><au>Tao, Qi</au><au>Zhao, He-Ping</au><au>Liang, Yongchao</au><au>Banerjee, Samiran</au><au>Li, Tingqiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Core Microbiota in the Rhizosphere of Heavy Metal Accumulators and Its Contribution to Plant Performance</atitle><jtitle>Environmental science & technology</jtitle><addtitle>Environ. 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Several keystone taxa in the rhizosphere networks were part of the core microbiota, the abundance of which was an important predictor of plant Cd accumulation. Furthermore, an inoculation experiment with synthetic communities comprising isolates belonging to the shared cores indicated that core microorganisms could facilitate plant growth and metal tolerance. Using RNA-based stable isotope probing, we discovered that abundant core taxa overlapped with active rhizobacteria utilizing root exudates, implying that the core rhizosphere microbiota assimilating plant-derived carbon may provide benefits to plant growth and host phenotype such as Cd accumulation. Our study suggests common principles underpinning hyperaccumulator–microbiome interactions, where plants consistently interact with a core set of microbes contributing to host fitness and plant performance. 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subjects | Accumulation Accumulators Cadmium Contaminants in Aquatic and Terrestrial Environments Cores Exudates Exudation Fitness Heavy metals Host plants Inoculation Microbiomes Microbiota Microorganisms Phenotypes Phylogeny Plant growth Plants Rhizosphere Stable isotopes Symbiosis |
title | Core Microbiota in the Rhizosphere of Heavy Metal Accumulators and Its Contribution to Plant Performance |
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