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Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes
Phenazines are natural bacterial antibiotics that can protect crops from disease. However, for most crops it is unknown which producers and specific phenazines are ecologically relevant, and whether phenazine biodegradation can counter their effects. To better understand their ecology, we developed...
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description | Phenazines are natural bacterial antibiotics that can protect crops from disease. However, for most crops it is unknown which producers and specific phenazines are ecologically relevant, and whether phenazine biodegradation can counter their effects. To better understand their ecology, we developed and environmentally-validated a quantitative metagenomic approach to mine for phenazine biosynthesis and biodegradation genes, applying it to >800 soil and plant-associated shotgun-metagenomes. We discover novel producer-crop associations and demonstrate that phenazine biosynthesis is prevalent across habitats and preferentially enriched in rhizospheres, whereas biodegrading bacteria are rare. We validate an association between maize and
, a putative producer abundant in crop microbiomes.
upregulates phenazine biosynthesis during phosphate limitation and robustly colonizes maize seedling roots. This work provides a global picture of phenazines in natural environments and highlights plant-microbe associations of agricultural potential. Our metagenomic approach may be extended to other metabolites and functional traits in diverse ecosystems. |
doi_str_mv | 10.7554/eLife.59726 |
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, a putative producer abundant in crop microbiomes.
upregulates phenazine biosynthesis during phosphate limitation and robustly colonizes maize seedling roots. This work provides a global picture of phenazines in natural environments and highlights plant-microbe associations of agricultural potential. Our metagenomic approach may be extended to other metabolites and functional traits in diverse ecosystems.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/eLife.59726</identifier><identifier>PMID: 32930660</identifier><language>eng</language><publisher>England: eLife Science Publications, Ltd</publisher><subject>Agricultural industry ; Agriculture ; Antibiotics ; Bacteria ; Biodegradation ; Biodegradation, Environmental ; Crops, Agricultural - microbiology ; Dyella japonica ; Ecology ; Ecosystems ; Gammaproteobacteria - physiology ; Metagenomics ; Microbiology and Infectious Disease ; Microbiota ; phenazines ; Phenazines - metabolism ; Physiological aspects ; Soil - chemistry ; Soil Microbiology ; Soil Pollutants - metabolism ; Soils ; Species Specificity ; Up-Regulation ; Zea mays - microbiology</subject><ispartof>eLife, 2020-09, Vol.9</ispartof><rights>2020, Dar et al.</rights><rights>COPYRIGHT 2020 eLife Science Publications, Ltd.</rights><rights>2020, Dar et al 2020 Dar et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c548t-c6e1db7d429637441db2bbade4c03f0771d289fb69156498e74b29a7b032e6653</citedby><cites>FETCH-LOGICAL-c548t-c6e1db7d429637441db2bbade4c03f0771d289fb69156498e74b29a7b032e6653</cites><orcidid>0000-0003-1647-1918 ; 0000-0002-6650-5488</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7591250/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7591250/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32930660$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dar, Daniel</creatorcontrib><creatorcontrib>Thomashow, Linda S</creatorcontrib><creatorcontrib>Weller, David M</creatorcontrib><creatorcontrib>Newman, Dianne K</creatorcontrib><title>Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes</title><title>eLife</title><addtitle>Elife</addtitle><description>Phenazines are natural bacterial antibiotics that can protect crops from disease. However, for most crops it is unknown which producers and specific phenazines are ecologically relevant, and whether phenazine biodegradation can counter their effects. To better understand their ecology, we developed and environmentally-validated a quantitative metagenomic approach to mine for phenazine biosynthesis and biodegradation genes, applying it to >800 soil and plant-associated shotgun-metagenomes. We discover novel producer-crop associations and demonstrate that phenazine biosynthesis is prevalent across habitats and preferentially enriched in rhizospheres, whereas biodegrading bacteria are rare. We validate an association between maize and
, a putative producer abundant in crop microbiomes.
upregulates phenazine biosynthesis during phosphate limitation and robustly colonizes maize seedling roots. This work provides a global picture of phenazines in natural environments and highlights plant-microbe associations of agricultural potential. Our metagenomic approach may be extended to other metabolites and functional traits in diverse ecosystems.</description><subject>Agricultural industry</subject><subject>Agriculture</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Biodegradation</subject><subject>Biodegradation, Environmental</subject><subject>Crops, Agricultural - microbiology</subject><subject>Dyella japonica</subject><subject>Ecology</subject><subject>Ecosystems</subject><subject>Gammaproteobacteria - physiology</subject><subject>Metagenomics</subject><subject>Microbiology and Infectious Disease</subject><subject>Microbiota</subject><subject>phenazines</subject><subject>Phenazines - metabolism</subject><subject>Physiological aspects</subject><subject>Soil - chemistry</subject><subject>Soil Microbiology</subject><subject>Soil Pollutants - metabolism</subject><subject>Soils</subject><subject>Species Specificity</subject><subject>Up-Regulation</subject><subject>Zea mays - microbiology</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNptkk1r3DAQhk1paUKaU-9F0FMp3sqyLFmXQghtsrBQ6Af0JvQx9irYkpG8Ickf6d-Ndt2GLFQ6jDR65h2NNEXxtsIr3jT0E2xcB6tGcMJeFKcEN7jELf398tn6pDhP6QbnwWnbVuJ1cVITUWPG8Gnx52oIWg1oUN4moyZAoUPTFrx6cB6QdiHd-3kLySWUkb3DQh-VVbMLHkW4BTUklCYwDlJ5sJ0zyIQhePewUJOaZ4g-IeeR6qMzu2HexZw1BTcsuiaGCY0um5xhhPSmeNVlYTj_a8-KX1-__Ly8LjffrtaXF5vSNLSdS8OgsppbSgSrOaV5Q7RWFqjBdYc5ryxpRaeZqBpGRQucaiIU17gmwFhTnxXrRdcGdSOn6EYV72VQTh4cIfZSxdmZAaRhugVmsdbAKG_zUxradqKylGlO6F7r86I17fQI1oCfc5FHoscn3m1lH24lb0RFGpwF3i8Cvcr5nO9CxszokpEXrBasqjEmmVr9h8rTQn7A4KFz2X8U8OEoIDMz3M292qUk1z--H7MfFzb_REoRuqfrV1juO04eOk4eOi7T755X_MT-66_6ESxp1No</recordid><startdate>20200915</startdate><enddate>20200915</enddate><creator>Dar, Daniel</creator><creator>Thomashow, Linda S</creator><creator>Weller, David M</creator><creator>Newman, Dianne K</creator><general>eLife Science Publications, Ltd</general><general>eLife Sciences Publications, Ltd</general><general>eLife Sciences Publications Ltd</general><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>ISR</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-1647-1918</orcidid><orcidid>https://orcid.org/0000-0002-6650-5488</orcidid></search><sort><creationdate>20200915</creationdate><title>Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes</title><author>Dar, Daniel ; Thomashow, Linda S ; Weller, David M ; Newman, Dianne K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c548t-c6e1db7d429637441db2bbade4c03f0771d289fb69156498e74b29a7b032e6653</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Agricultural industry</topic><topic>Agriculture</topic><topic>Antibiotics</topic><topic>Bacteria</topic><topic>Biodegradation</topic><topic>Biodegradation, Environmental</topic><topic>Crops, Agricultural - microbiology</topic><topic>Dyella japonica</topic><topic>Ecology</topic><topic>Ecosystems</topic><topic>Gammaproteobacteria - physiology</topic><topic>Metagenomics</topic><topic>Microbiology and Infectious Disease</topic><topic>Microbiota</topic><topic>phenazines</topic><topic>Phenazines - metabolism</topic><topic>Physiological aspects</topic><topic>Soil - chemistry</topic><topic>Soil Microbiology</topic><topic>Soil Pollutants - metabolism</topic><topic>Soils</topic><topic>Species Specificity</topic><topic>Up-Regulation</topic><topic>Zea mays - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dar, Daniel</creatorcontrib><creatorcontrib>Thomashow, Linda S</creatorcontrib><creatorcontrib>Weller, David M</creatorcontrib><creatorcontrib>Newman, Dianne K</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>eLife</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dar, Daniel</au><au>Thomashow, Linda S</au><au>Weller, David M</au><au>Newman, Dianne K</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes</atitle><jtitle>eLife</jtitle><addtitle>Elife</addtitle><date>2020-09-15</date><risdate>2020</risdate><volume>9</volume><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>Phenazines are natural bacterial antibiotics that can protect crops from disease. However, for most crops it is unknown which producers and specific phenazines are ecologically relevant, and whether phenazine biodegradation can counter their effects. To better understand their ecology, we developed and environmentally-validated a quantitative metagenomic approach to mine for phenazine biosynthesis and biodegradation genes, applying it to >800 soil and plant-associated shotgun-metagenomes. We discover novel producer-crop associations and demonstrate that phenazine biosynthesis is prevalent across habitats and preferentially enriched in rhizospheres, whereas biodegrading bacteria are rare. We validate an association between maize and
, a putative producer abundant in crop microbiomes.
upregulates phenazine biosynthesis during phosphate limitation and robustly colonizes maize seedling roots. This work provides a global picture of phenazines in natural environments and highlights plant-microbe associations of agricultural potential. Our metagenomic approach may be extended to other metabolites and functional traits in diverse ecosystems.</abstract><cop>England</cop><pub>eLife Science Publications, Ltd</pub><pmid>32930660</pmid><doi>10.7554/eLife.59726</doi><orcidid>https://orcid.org/0000-0003-1647-1918</orcidid><orcidid>https://orcid.org/0000-0002-6650-5488</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Agricultural industry Agriculture Antibiotics Bacteria Biodegradation Biodegradation, Environmental Crops, Agricultural - microbiology Dyella japonica Ecology Ecosystems Gammaproteobacteria - physiology Metagenomics Microbiology and Infectious Disease Microbiota phenazines Phenazines - metabolism Physiological aspects Soil - chemistry Soil Microbiology Soil Pollutants - metabolism Soils Species Specificity Up-Regulation Zea mays - microbiology |
title | Global landscape of phenazine biosynthesis and biodegradation reveals species-specific colonization patterns in agricultural soils and crop microbiomes |
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