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Microbial biodegradation of biuret: defining biuret hydrolases within the isochorismatase superfamily
Summary Biuret is a minor component of urea fertilizer and an intermediate in s‐triazine herbicide biodegradation. The microbial metabolism of biuret has never been comprehensively studied. Here, we enriched and isolated bacteria from a potato field that grew on biuret as a sole nitrogen source. We...
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Published in: | Environmental microbiology 2018-06, Vol.20 (6), p.2099-2111 |
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creator | Robinson, Serina L. Badalamenti, Jonathan P. Dodge, Anthony G. Tassoulas, Lambros J. Wackett, Lawrence P. |
description | Summary
Biuret is a minor component of urea fertilizer and an intermediate in s‐triazine herbicide biodegradation. The microbial metabolism of biuret has never been comprehensively studied. Here, we enriched and isolated bacteria from a potato field that grew on biuret as a sole nitrogen source. We sequenced the genome of the fastest‐growing isolate, Herbaspirillum sp. BH‐1 and identified genes encoding putative biuret hydrolases (BHs). We purified and characterized a functional BH enzyme from Herbaspirillum sp. BH‐1 and two other bacteria from divergent phyla. The BH enzymes reacted exclusively with biuret in the range of 2‐11 µmol min−1 mg−1 protein. We then constructed a global protein superfamily network to map structure‐function relationships in the BH subfamily and used this to mine > 7000 genomes. High‐confidence BH sequences were detected in Actinobacteria, Alpha‐ and Beta‐proteobacteria, and some fungi, archaea and green algae, but not animals or land plants. Unexpectedly, no cyanuric acid hydrolase homologs were detected in > 90% of genomes with BH homologs, suggesting BHs may have arisen independently of s‐triazine ring metabolism. This work links genotype to phenotype by enabling accurate genome‐mining to predict microbial utilization of biuret. Importantly, it advances understanding of the microbial capacity for biuret biodegradation in agricultural systems. |
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Biuret is a minor component of urea fertilizer and an intermediate in s‐triazine herbicide biodegradation. The microbial metabolism of biuret has never been comprehensively studied. Here, we enriched and isolated bacteria from a potato field that grew on biuret as a sole nitrogen source. We sequenced the genome of the fastest‐growing isolate, Herbaspirillum sp. BH‐1 and identified genes encoding putative biuret hydrolases (BHs). We purified and characterized a functional BH enzyme from Herbaspirillum sp. BH‐1 and two other bacteria from divergent phyla. The BH enzymes reacted exclusively with biuret in the range of 2‐11 µmol min−1 mg−1 protein. We then constructed a global protein superfamily network to map structure‐function relationships in the BH subfamily and used this to mine > 7000 genomes. High‐confidence BH sequences were detected in Actinobacteria, Alpha‐ and Beta‐proteobacteria, and some fungi, archaea and green algae, but not animals or land plants. Unexpectedly, no cyanuric acid hydrolase homologs were detected in > 90% of genomes with BH homologs, suggesting BHs may have arisen independently of s‐triazine ring metabolism. This work links genotype to phenotype by enabling accurate genome‐mining to predict microbial utilization of biuret. Importantly, it advances understanding of the microbial capacity for biuret biodegradation in agricultural systems.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.14094</identifier><identifier>PMID: 29528550</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Agrochemicals ; Algae ; Aquatic plants ; Archaea ; Bacteria ; Biodegradation ; Capacity ; Cyanuric acid ; Fertilizers ; Fungi ; Gene sequencing ; Genomes ; Genotypes ; Herbicides ; Homology ; Hydrolase ; Hydrolases ; Isochorismatase ; Metabolism ; Microorganisms ; Phenotypes ; Potatoes ; Proteins ; Rings (mathematics) ; Structure-function relationships ; Triazine ; Urea</subject><ispartof>Environmental microbiology, 2018-06, Vol.20 (6), p.2099-2111</ispartof><rights>2018 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2018 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4374-d13fe12a2a4a6dd4c7c2d9417cb0972eae033d6adc2d5930ffb5cafcdf3b8f4a3</citedby><cites>FETCH-LOGICAL-c4374-d13fe12a2a4a6dd4c7c2d9417cb0972eae033d6adc2d5930ffb5cafcdf3b8f4a3</cites><orcidid>0000-0001-6947-7913 ; 0000-0001-8988-7717</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27922,27923</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29528550$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Robinson, Serina L.</creatorcontrib><creatorcontrib>Badalamenti, Jonathan P.</creatorcontrib><creatorcontrib>Dodge, Anthony G.</creatorcontrib><creatorcontrib>Tassoulas, Lambros J.</creatorcontrib><creatorcontrib>Wackett, Lawrence P.</creatorcontrib><title>Microbial biodegradation of biuret: defining biuret hydrolases within the isochorismatase superfamily</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Biuret is a minor component of urea fertilizer and an intermediate in s‐triazine herbicide biodegradation. The microbial metabolism of biuret has never been comprehensively studied. Here, we enriched and isolated bacteria from a potato field that grew on biuret as a sole nitrogen source. We sequenced the genome of the fastest‐growing isolate, Herbaspirillum sp. BH‐1 and identified genes encoding putative biuret hydrolases (BHs). We purified and characterized a functional BH enzyme from Herbaspirillum sp. BH‐1 and two other bacteria from divergent phyla. The BH enzymes reacted exclusively with biuret in the range of 2‐11 µmol min−1 mg−1 protein. We then constructed a global protein superfamily network to map structure‐function relationships in the BH subfamily and used this to mine > 7000 genomes. High‐confidence BH sequences were detected in Actinobacteria, Alpha‐ and Beta‐proteobacteria, and some fungi, archaea and green algae, but not animals or land plants. Unexpectedly, no cyanuric acid hydrolase homologs were detected in > 90% of genomes with BH homologs, suggesting BHs may have arisen independently of s‐triazine ring metabolism. This work links genotype to phenotype by enabling accurate genome‐mining to predict microbial utilization of biuret. Importantly, it advances understanding of the microbial capacity for biuret biodegradation in agricultural systems.</description><subject>Agrochemicals</subject><subject>Algae</subject><subject>Aquatic plants</subject><subject>Archaea</subject><subject>Bacteria</subject><subject>Biodegradation</subject><subject>Capacity</subject><subject>Cyanuric acid</subject><subject>Fertilizers</subject><subject>Fungi</subject><subject>Gene sequencing</subject><subject>Genomes</subject><subject>Genotypes</subject><subject>Herbicides</subject><subject>Homology</subject><subject>Hydrolase</subject><subject>Hydrolases</subject><subject>Isochorismatase</subject><subject>Metabolism</subject><subject>Microorganisms</subject><subject>Phenotypes</subject><subject>Potatoes</subject><subject>Proteins</subject><subject>Rings (mathematics)</subject><subject>Structure-function relationships</subject><subject>Triazine</subject><subject>Urea</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNqFkb1PwzAQxS0EoqUws6FILCyl_krTsKGqQKVWLDBbjn1uXSVxsRNV-e9xaenAgpez3_3uyXqH0C3BjySeEeFjOqQ5jU-Oc36G-ifl_HQntIeuQthgTDKW4UvUo3lKJ2mK-wiWVnlXWFkmhXUaVl5q2VhXJ85EpfXQPCUajK1tvToKybrT3pUyQEh2tlnbOmnWkNjg1Np5GyrZxF4S2i14IytbdtfowsgywM2xDtDny-xj-jZcvL_Op8-LoeIs40NNmAFCJZVcjrXmKlNU55xkqsB5RkECZkyPpY5ymjNsTJEqaZQ2rJgYLtkAPRx8t959tRAaUdmgoCxlDa4NgmLCCOYpoRG9_4NuXOvr-LtITXLG03G-p0YHKoYUggcjtt5W0neCYLHfgNhnLPZ5i58NxIm7o29bVKBP_G_kEUgPwM6W0P3nJ2bL-cH4G3DTkjk</recordid><startdate>201806</startdate><enddate>201806</enddate><creator>Robinson, Serina L.</creator><creator>Badalamenti, Jonathan P.</creator><creator>Dodge, Anthony G.</creator><creator>Tassoulas, Lambros J.</creator><creator>Wackett, Lawrence P.</creator><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-6947-7913</orcidid><orcidid>https://orcid.org/0000-0001-8988-7717</orcidid></search><sort><creationdate>201806</creationdate><title>Microbial biodegradation of biuret: defining biuret hydrolases within the isochorismatase superfamily</title><author>Robinson, Serina L. ; Badalamenti, Jonathan P. ; Dodge, Anthony G. ; Tassoulas, Lambros J. ; Wackett, Lawrence P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4374-d13fe12a2a4a6dd4c7c2d9417cb0972eae033d6adc2d5930ffb5cafcdf3b8f4a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Agrochemicals</topic><topic>Algae</topic><topic>Aquatic plants</topic><topic>Archaea</topic><topic>Bacteria</topic><topic>Biodegradation</topic><topic>Capacity</topic><topic>Cyanuric acid</topic><topic>Fertilizers</topic><topic>Fungi</topic><topic>Gene sequencing</topic><topic>Genomes</topic><topic>Genotypes</topic><topic>Herbicides</topic><topic>Homology</topic><topic>Hydrolase</topic><topic>Hydrolases</topic><topic>Isochorismatase</topic><topic>Metabolism</topic><topic>Microorganisms</topic><topic>Phenotypes</topic><topic>Potatoes</topic><topic>Proteins</topic><topic>Rings (mathematics)</topic><topic>Structure-function relationships</topic><topic>Triazine</topic><topic>Urea</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Robinson, Serina L.</creatorcontrib><creatorcontrib>Badalamenti, Jonathan P.</creatorcontrib><creatorcontrib>Dodge, Anthony G.</creatorcontrib><creatorcontrib>Tassoulas, Lambros J.</creatorcontrib><creatorcontrib>Wackett, Lawrence P.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Robinson, Serina L.</au><au>Badalamenti, Jonathan P.</au><au>Dodge, Anthony G.</au><au>Tassoulas, Lambros J.</au><au>Wackett, Lawrence P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microbial biodegradation of biuret: defining biuret hydrolases within the isochorismatase superfamily</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2018-06</date><risdate>2018</risdate><volume>20</volume><issue>6</issue><spage>2099</spage><epage>2111</epage><pages>2099-2111</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Biuret is a minor component of urea fertilizer and an intermediate in s‐triazine herbicide biodegradation. The microbial metabolism of biuret has never been comprehensively studied. Here, we enriched and isolated bacteria from a potato field that grew on biuret as a sole nitrogen source. We sequenced the genome of the fastest‐growing isolate, Herbaspirillum sp. BH‐1 and identified genes encoding putative biuret hydrolases (BHs). We purified and characterized a functional BH enzyme from Herbaspirillum sp. BH‐1 and two other bacteria from divergent phyla. The BH enzymes reacted exclusively with biuret in the range of 2‐11 µmol min−1 mg−1 protein. We then constructed a global protein superfamily network to map structure‐function relationships in the BH subfamily and used this to mine > 7000 genomes. High‐confidence BH sequences were detected in Actinobacteria, Alpha‐ and Beta‐proteobacteria, and some fungi, archaea and green algae, but not animals or land plants. Unexpectedly, no cyanuric acid hydrolase homologs were detected in > 90% of genomes with BH homologs, suggesting BHs may have arisen independently of s‐triazine ring metabolism. This work links genotype to phenotype by enabling accurate genome‐mining to predict microbial utilization of biuret. Importantly, it advances understanding of the microbial capacity for biuret biodegradation in agricultural systems.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>29528550</pmid><doi>10.1111/1462-2920.14094</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-6947-7913</orcidid><orcidid>https://orcid.org/0000-0001-8988-7717</orcidid></addata></record> |
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subjects | Agrochemicals Algae Aquatic plants Archaea Bacteria Biodegradation Capacity Cyanuric acid Fertilizers Fungi Gene sequencing Genomes Genotypes Herbicides Homology Hydrolase Hydrolases Isochorismatase Metabolism Microorganisms Phenotypes Potatoes Proteins Rings (mathematics) Structure-function relationships Triazine Urea |
title | Microbial biodegradation of biuret: defining biuret hydrolases within the isochorismatase superfamily |
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