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Metagenomic insights into the RDX-degrading potential of the ovine rumen microbiome
The manufacturing processes of royal demolition explosive (RDX), or hexahydro-1,3,5-trinitro-1,3,5-triazine, have resulted in serious water contamination. As a potential carcinogen, RDX can cause a broad range of harmful effects to humans and animals. The ovine rumen is capable of rapid degradation...
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Published in: | PloS one 2014-11, Vol.9 (11), p.e110505 |
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description | The manufacturing processes of royal demolition explosive (RDX), or hexahydro-1,3,5-trinitro-1,3,5-triazine, have resulted in serious water contamination. As a potential carcinogen, RDX can cause a broad range of harmful effects to humans and animals. The ovine rumen is capable of rapid degradation of nitroaromatic compounds, including RDX. While ruminal RDX-degrading bacteria have been identified, the genes and pathways responsible for RDX degradation in the rumen have yet to be characterized. In this study, we characterized the metabolic potential of the ovine rumen using metagenomic approaches. Sequences homologous to at least five RDX-degrading genes cloned from environmental samples (diaA, xenA, xenB, xplA, and xplB) were present in the ovine rumen microbiome. Among them, diaA was the most abundant, likely reflective of the predominance of the genus Clostridium in the ovine rumen. At least ten genera known to harbor RDX-degrading microorganisms were detectable. Metagenomic sequences were also annotated using public databases, such as Pfam, COG, and KEGG. Five of the six Pfam protein families known to be responsible for RDX degradation in environmental samples were identified in the ovine rumen. However, increased substrate availability did not appear to enhance the proliferation of RDX-degrading bacteria and alter the microbial composition of the ovine rumen. This implies that the RDX-degrading capacity of the ovine rumen microbiome is likely regulated at the transcription level. Our results provide metagenomic insights into the RDX-degrading potential of the ovine rumen, and they will facilitate the development of novel and economic bioremediation strategies. |
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As a potential carcinogen, RDX can cause a broad range of harmful effects to humans and animals. The ovine rumen is capable of rapid degradation of nitroaromatic compounds, including RDX. While ruminal RDX-degrading bacteria have been identified, the genes and pathways responsible for RDX degradation in the rumen have yet to be characterized. In this study, we characterized the metabolic potential of the ovine rumen using metagenomic approaches. Sequences homologous to at least five RDX-degrading genes cloned from environmental samples (diaA, xenA, xenB, xplA, and xplB) were present in the ovine rumen microbiome. Among them, diaA was the most abundant, likely reflective of the predominance of the genus Clostridium in the ovine rumen. At least ten genera known to harbor RDX-degrading microorganisms were detectable. Metagenomic sequences were also annotated using public databases, such as Pfam, COG, and KEGG. Five of the six Pfam protein families known to be responsible for RDX degradation in environmental samples were identified in the ovine rumen. However, increased substrate availability did not appear to enhance the proliferation of RDX-degrading bacteria and alter the microbial composition of the ovine rumen. This implies that the RDX-degrading capacity of the ovine rumen microbiome is likely regulated at the transcription level. Our results provide metagenomic insights into the RDX-degrading potential of the ovine rumen, and they will facilitate the development of novel and economic bioremediation strategies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0110505</identifier><identifier>PMID: 25383623</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Animals ; Bacteria ; Base Sequence ; Biodegradation ; Biodegradation, Environmental ; Bioinformatics ; Biology and Life Sciences ; Bioremediation ; Carcinogens ; Cloning ; Cloning, Molecular ; Clostridium ; Contamination ; Cytochrome ; Demolition ; Ecology and Environmental Sciences ; Environmental degradation ; Enzymes ; Gene expression ; Gene sequencing ; Genes ; Genes, Bacterial - genetics ; Genomes ; Genomics ; Groundwater ; Hexahydro-1,3,5-trinitro-1,3,5-triazine ; Homology ; Male ; Manufacturing industry ; Metabolism ; Metagenomics - methods ; Microbiota ; Microbiota - genetics ; Microbiota - physiology ; Microorganisms ; Molecular Sequence Annotation ; Molecular Sequence Data ; Nitroaromatic compounds ; Protein families ; Proteins ; RDX ; RNA, Ribosomal, 16S - genetics ; Rumen ; Rumen - microbiology ; Sequence Analysis, DNA ; Sheep ; Sheep - microbiology ; Substrates ; Transcription ; Triazine ; Triazines - metabolism ; Veterinary colleges ; Veterinary medicine ; Water Pollutants, Chemical - metabolism ; Water pollution</subject><ispartof>PloS one, 2014-11, Vol.9 (11), p.e110505</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-c795cd061878f75409c9a87c219ac399210f807ee9ac46d9bbe45c741997702c3</citedby><cites>FETCH-LOGICAL-c692t-c795cd061878f75409c9a87c219ac399210f807ee9ac46d9bbe45c741997702c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1622299487/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1622299487?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,44566,53766,53768,74869</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25383623$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Friedberg, Iddo</contributor><creatorcontrib>Li, Robert W</creatorcontrib><creatorcontrib>Giarrizzo, Juan Gabriel</creatorcontrib><creatorcontrib>Wu, Sitao</creatorcontrib><creatorcontrib>Li, Weizhong</creatorcontrib><creatorcontrib>Duringer, Jennifer M</creatorcontrib><creatorcontrib>Craig, A Morrie</creatorcontrib><title>Metagenomic insights into the RDX-degrading potential of the ovine rumen microbiome</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The manufacturing processes of royal demolition explosive (RDX), or hexahydro-1,3,5-trinitro-1,3,5-triazine, have resulted in serious water contamination. As a potential carcinogen, RDX can cause a broad range of harmful effects to humans and animals. The ovine rumen is capable of rapid degradation of nitroaromatic compounds, including RDX. While ruminal RDX-degrading bacteria have been identified, the genes and pathways responsible for RDX degradation in the rumen have yet to be characterized. In this study, we characterized the metabolic potential of the ovine rumen using metagenomic approaches. Sequences homologous to at least five RDX-degrading genes cloned from environmental samples (diaA, xenA, xenB, xplA, and xplB) were present in the ovine rumen microbiome. Among them, diaA was the most abundant, likely reflective of the predominance of the genus Clostridium in the ovine rumen. At least ten genera known to harbor RDX-degrading microorganisms were detectable. Metagenomic sequences were also annotated using public databases, such as Pfam, COG, and KEGG. Five of the six Pfam protein families known to be responsible for RDX degradation in environmental samples were identified in the ovine rumen. However, increased substrate availability did not appear to enhance the proliferation of RDX-degrading bacteria and alter the microbial composition of the ovine rumen. This implies that the RDX-degrading capacity of the ovine rumen microbiome is likely regulated at the transcription level. Our results provide metagenomic insights into the RDX-degrading potential of the ovine rumen, and they will facilitate the development of novel and economic bioremediation strategies.</description><subject>Acids</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Base Sequence</subject><subject>Biodegradation</subject><subject>Biodegradation, Environmental</subject><subject>Bioinformatics</subject><subject>Biology and Life Sciences</subject><subject>Bioremediation</subject><subject>Carcinogens</subject><subject>Cloning</subject><subject>Cloning, Molecular</subject><subject>Clostridium</subject><subject>Contamination</subject><subject>Cytochrome</subject><subject>Demolition</subject><subject>Ecology and Environmental Sciences</subject><subject>Environmental degradation</subject><subject>Enzymes</subject><subject>Gene expression</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genes, Bacterial - genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Groundwater</subject><subject>Hexahydro-1,3,5-trinitro-1,3,5-triazine</subject><subject>Homology</subject><subject>Male</subject><subject>Manufacturing industry</subject><subject>Metabolism</subject><subject>Metagenomics - methods</subject><subject>Microbiota</subject><subject>Microbiota - genetics</subject><subject>Microbiota - physiology</subject><subject>Microorganisms</subject><subject>Molecular Sequence Annotation</subject><subject>Molecular Sequence Data</subject><subject>Nitroaromatic compounds</subject><subject>Protein families</subject><subject>Proteins</subject><subject>RDX</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Rumen</subject><subject>Rumen - microbiology</subject><subject>Sequence Analysis, DNA</subject><subject>Sheep</subject><subject>Sheep - microbiology</subject><subject>Substrates</subject><subject>Transcription</subject><subject>Triazine</subject><subject>Triazines - metabolism</subject><subject>Veterinary colleges</subject><subject>Veterinary medicine</subject><subject>Water Pollutants, Chemical - metabolism</subject><subject>Water pollution</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl1rFDEUhgdRbK3-A9EBQfBi13xNMrkRSv1aqBRaFe9CNnNmNmUmWZNM0X9vtjstO6AguZgzyXPeHN68RfEcoyWmAr-99mNwul9uvYMlwhhVqHpQHGNJyYITRB8e1EfFkxivEapozfnj4ojkgnJCj4urL5B0B84P1pTWRdttUsxF8mXaQHn5_seigS7oxrqu3PoELlndl769PfY31kEZxgFcmQWCX1s_wNPiUav7CM-m70nx7eOHr2efF-cXn1Znp-cLwyVJCyNkZRrEcS3qVlQMSSN1LQzBUhsqJcGorZEAyL-MN3K9BlYZwbCUQiBi6Enxcq-77X1Ukx9RYU4IkZLVIhOrPdF4fa22wQ46_FZeW3W74UOndEjW9KBaIAxMS9uKmlwI2eRLCauZwEAb3WStd9Nt43qAxmQngu5novMTZzeq8zeKEcIZ3w3zahII_ucIMf1j5InqdJ7KutZnMTPYaNQpwzWnlRA4U8u_UHk1kN8hJ6K1eX_W8GbWkJkEv1KnxxjV6ury_9mL73P29QG7Ad2nTfT9mKx3cQ6yPZhTEmOA9t45jNQu0HduqF2g1RTo3Pbi0PX7prsE0z-kffBa</recordid><startdate>20141110</startdate><enddate>20141110</enddate><creator>Li, Robert W</creator><creator>Giarrizzo, Juan Gabriel</creator><creator>Wu, Sitao</creator><creator>Li, Weizhong</creator><creator>Duringer, Jennifer M</creator><creator>Craig, A Morrie</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20141110</creationdate><title>Metagenomic insights into the RDX-degrading potential of the ovine rumen microbiome</title><author>Li, Robert W ; Giarrizzo, Juan Gabriel ; Wu, Sitao ; Li, Weizhong ; Duringer, Jennifer M ; Craig, A Morrie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-c795cd061878f75409c9a87c219ac399210f807ee9ac46d9bbe45c741997702c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Acids</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Base Sequence</topic><topic>Biodegradation</topic><topic>Biodegradation, Environmental</topic><topic>Bioinformatics</topic><topic>Biology and Life Sciences</topic><topic>Bioremediation</topic><topic>Carcinogens</topic><topic>Cloning</topic><topic>Cloning, Molecular</topic><topic>Clostridium</topic><topic>Contamination</topic><topic>Cytochrome</topic><topic>Demolition</topic><topic>Ecology and Environmental Sciences</topic><topic>Environmental degradation</topic><topic>Enzymes</topic><topic>Gene expression</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Genes, Bacterial - genetics</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Groundwater</topic><topic>Hexahydro-1,3,5-trinitro-1,3,5-triazine</topic><topic>Homology</topic><topic>Male</topic><topic>Manufacturing industry</topic><topic>Metabolism</topic><topic>Metagenomics - methods</topic><topic>Microbiota</topic><topic>Microbiota - genetics</topic><topic>Microbiota - physiology</topic><topic>Microorganisms</topic><topic>Molecular Sequence Annotation</topic><topic>Molecular Sequence Data</topic><topic>Nitroaromatic compounds</topic><topic>Protein families</topic><topic>Proteins</topic><topic>RDX</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Rumen</topic><topic>Rumen - microbiology</topic><topic>Sequence Analysis, DNA</topic><topic>Sheep</topic><topic>Sheep - microbiology</topic><topic>Substrates</topic><topic>Transcription</topic><topic>Triazine</topic><topic>Triazines - metabolism</topic><topic>Veterinary colleges</topic><topic>Veterinary medicine</topic><topic>Water Pollutants, Chemical - 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As a potential carcinogen, RDX can cause a broad range of harmful effects to humans and animals. The ovine rumen is capable of rapid degradation of nitroaromatic compounds, including RDX. While ruminal RDX-degrading bacteria have been identified, the genes and pathways responsible for RDX degradation in the rumen have yet to be characterized. In this study, we characterized the metabolic potential of the ovine rumen using metagenomic approaches. Sequences homologous to at least five RDX-degrading genes cloned from environmental samples (diaA, xenA, xenB, xplA, and xplB) were present in the ovine rumen microbiome. Among them, diaA was the most abundant, likely reflective of the predominance of the genus Clostridium in the ovine rumen. At least ten genera known to harbor RDX-degrading microorganisms were detectable. Metagenomic sequences were also annotated using public databases, such as Pfam, COG, and KEGG. Five of the six Pfam protein families known to be responsible for RDX degradation in environmental samples were identified in the ovine rumen. However, increased substrate availability did not appear to enhance the proliferation of RDX-degrading bacteria and alter the microbial composition of the ovine rumen. This implies that the RDX-degrading capacity of the ovine rumen microbiome is likely regulated at the transcription level. Our results provide metagenomic insights into the RDX-degrading potential of the ovine rumen, and they will facilitate the development of novel and economic bioremediation strategies.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25383623</pmid><doi>10.1371/journal.pone.0110505</doi><oa>free_for_read</oa></addata></record> |
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subjects | Acids Animals Bacteria Base Sequence Biodegradation Biodegradation, Environmental Bioinformatics Biology and Life Sciences Bioremediation Carcinogens Cloning Cloning, Molecular Clostridium Contamination Cytochrome Demolition Ecology and Environmental Sciences Environmental degradation Enzymes Gene expression Gene sequencing Genes Genes, Bacterial - genetics Genomes Genomics Groundwater Hexahydro-1,3,5-trinitro-1,3,5-triazine Homology Male Manufacturing industry Metabolism Metagenomics - methods Microbiota Microbiota - genetics Microbiota - physiology Microorganisms Molecular Sequence Annotation Molecular Sequence Data Nitroaromatic compounds Protein families Proteins RDX RNA, Ribosomal, 16S - genetics Rumen Rumen - microbiology Sequence Analysis, DNA Sheep Sheep - microbiology Substrates Transcription Triazine Triazines - metabolism Veterinary colleges Veterinary medicine Water Pollutants, Chemical - metabolism Water pollution |
title | Metagenomic insights into the RDX-degrading potential of the ovine rumen microbiome |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-29T02%3A59%3A53IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Metagenomic%20insights%20into%20the%20RDX-degrading%20potential%20of%20the%20ovine%20rumen%20microbiome&rft.jtitle=PloS%20one&rft.au=Li,%20Robert%20W&rft.date=2014-11-10&rft.volume=9&rft.issue=11&rft.spage=e110505&rft.pages=e110505-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0110505&rft_dat=%3Cgale_plos_%3EA418635771%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c692t-c795cd061878f75409c9a87c219ac399210f807ee9ac46d9bbe45c741997702c3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1622299487&rft_id=info:pmid/25383623&rft_galeid=A418635771&rfr_iscdi=true |