Microbial metabolism of methanol and methylamine in the Gulf of Mexico: insight into marine carbon and nitrogen cycling
Summary One carbon (C1) metabolism plays an important role in marine carbon cycling but the dynamics and modes of C1 transformations are not fully understood. We made contemporaneous measurements of methylamine and methanol metabolism to elucidate the role of C1 compounds as sources of carbon, energ...
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Veröffentlicht in: | Environmental microbiology 2018-12, Vol.20 (12), p.4543-4554 |
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creator | Zhuang, Guang‐Chao Peña‐Montenegro, Tito D. Montgomery, Andrew Hunter, Kimberley S. Joye, Samantha B. |
description | Summary
One carbon (C1) metabolism plays an important role in marine carbon cycling but the dynamics and modes of C1 transformations are not fully understood. We made contemporaneous measurements of methylamine and methanol metabolism to elucidate the role of C1 compounds as sources of carbon, energy and nitrogen. Methanol and methylamine were predominantly used as an energy source in offshore waters (oxidation rate constant: kmethanol: 0.02−0.10 day−1; kmethylamine: 0.01−0.18 day−1), but were also important sources of biomass carbon in coastal waters (assimilation rate constant: kmethanol: 0.04−0.10 day−1; kmethylamine: 0.01−0.05 day−1). The relative extent of assimilation versus oxidation for these substrates correlated positively with chlorophyll, nutrients and heterotrophic bacterial production. Methanol oxidation and assimilation were stimulated significantly by nutrient addition. In contrast, methylamine metabolism was inhibited by ammonium or nitrate, suggesting that methylamine served as a nitrogen source. A preliminary metagenomic survey revealed a diverse population of putative C1‐utilizing microorganisms. These results show that the remineralization of methylamine could provide both C and N sources for microbes. Both methanol and methylamine contribute to microbial energetic and carbon substrate demands with a distinctly different signature in nearshore versus offshore environments. |
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One carbon (C1) metabolism plays an important role in marine carbon cycling but the dynamics and modes of C1 transformations are not fully understood. We made contemporaneous measurements of methylamine and methanol metabolism to elucidate the role of C1 compounds as sources of carbon, energy and nitrogen. Methanol and methylamine were predominantly used as an energy source in offshore waters (oxidation rate constant: kmethanol: 0.02−0.10 day−1; kmethylamine: 0.01−0.18 day−1), but were also important sources of biomass carbon in coastal waters (assimilation rate constant: kmethanol: 0.04−0.10 day−1; kmethylamine: 0.01−0.05 day−1). The relative extent of assimilation versus oxidation for these substrates correlated positively with chlorophyll, nutrients and heterotrophic bacterial production. Methanol oxidation and assimilation were stimulated significantly by nutrient addition. In contrast, methylamine metabolism was inhibited by ammonium or nitrate, suggesting that methylamine served as a nitrogen source. A preliminary metagenomic survey revealed a diverse population of putative C1‐utilizing microorganisms. These results show that the remineralization of methylamine could provide both C and N sources for microbes. Both methanol and methylamine contribute to microbial energetic and carbon substrate demands with a distinctly different signature in nearshore versus offshore environments.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.14406</identifier><identifier>PMID: 30209867</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Ammonium ; Ammonium compounds ; Assimilation ; Carbon ; Carbon cycle ; Carbon sources ; Chlorophyll ; Chlorophylls ; Coastal waters ; Dynamics ; Metabolism ; Methanol ; Methylamine ; Microorganisms ; Mineral nutrients ; Nitrogen ; Nitrogen cycle ; Nutrients ; Offshore ; Oxidation ; Oxidation rate ; Remineralization ; Substrates ; Surveying</subject><ispartof>Environmental microbiology, 2018-12, Vol.20 (12), p.4543-4554</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-c3716-5551a78a9325466bf0a29b4cffce7a1b3b0b34f7fec2862c12b00d6b7457c15b3</citedby><cites>FETCH-LOGICAL-c3716-5551a78a9325466bf0a29b4cffce7a1b3b0b34f7fec2862c12b00d6b7457c15b3</cites><orcidid>0000-0003-1610-451X ; 0000-0002-2646-4183 ; 0000-0002-6282-8415</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%2F1462-2920.14406$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.14406$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30209867$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhuang, Guang‐Chao</creatorcontrib><creatorcontrib>Peña‐Montenegro, Tito D.</creatorcontrib><creatorcontrib>Montgomery, Andrew</creatorcontrib><creatorcontrib>Hunter, Kimberley S.</creatorcontrib><creatorcontrib>Joye, Samantha B.</creatorcontrib><title>Microbial metabolism of methanol and methylamine in the Gulf of Mexico: insight into marine carbon and nitrogen cycling</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
One carbon (C1) metabolism plays an important role in marine carbon cycling but the dynamics and modes of C1 transformations are not fully understood. We made contemporaneous measurements of methylamine and methanol metabolism to elucidate the role of C1 compounds as sources of carbon, energy and nitrogen. Methanol and methylamine were predominantly used as an energy source in offshore waters (oxidation rate constant: kmethanol: 0.02−0.10 day−1; kmethylamine: 0.01−0.18 day−1), but were also important sources of biomass carbon in coastal waters (assimilation rate constant: kmethanol: 0.04−0.10 day−1; kmethylamine: 0.01−0.05 day−1). The relative extent of assimilation versus oxidation for these substrates correlated positively with chlorophyll, nutrients and heterotrophic bacterial production. Methanol oxidation and assimilation were stimulated significantly by nutrient addition. In contrast, methylamine metabolism was inhibited by ammonium or nitrate, suggesting that methylamine served as a nitrogen source. A preliminary metagenomic survey revealed a diverse population of putative C1‐utilizing microorganisms. These results show that the remineralization of methylamine could provide both C and N sources for microbes. Both methanol and methylamine contribute to microbial energetic and carbon substrate demands with a distinctly different signature in nearshore versus offshore environments.</description><subject>Ammonium</subject><subject>Ammonium compounds</subject><subject>Assimilation</subject><subject>Carbon</subject><subject>Carbon cycle</subject><subject>Carbon sources</subject><subject>Chlorophyll</subject><subject>Chlorophylls</subject><subject>Coastal waters</subject><subject>Dynamics</subject><subject>Metabolism</subject><subject>Methanol</subject><subject>Methylamine</subject><subject>Microorganisms</subject><subject>Mineral nutrients</subject><subject>Nitrogen</subject><subject>Nitrogen cycle</subject><subject>Nutrients</subject><subject>Offshore</subject><subject>Oxidation</subject><subject>Oxidation rate</subject><subject>Remineralization</subject><subject>Substrates</subject><subject>Surveying</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNqFkcFPwyAUxonRuDk9ezNNvHiZA9rC6s0scy7Z4kXPBBhsLBRmaaP976Xb3MGLJOTxXn58ge8D4BbBRxTXCGUED3GBY5tlkJyB_mlyfjoj3ANXIWwhRDSl8BL0UohhMSa0D76WRlZeGG6TUtVceGtCmXjddRvuvE24W-2b1vLSOJUYl9Qblcwaqztuqb6N9E9xHMx6U8da-6TkVYdKXgnv9grO1JVfK5fIVlrj1tfgQnMb1M2xDsDHy_R98jpcvM3mk-fFUKYUkWGe54jTMS9SnGeECA05LkQmtZaKciRSAUWaaaqVxGOCJcICwhURNMupRLlIB-DhoLur_GejQs1KE6Syljvlm8Awgimh3Y7o_R9065vKxddFKs8KQqOVkRodqGhbCJXSbFeZ-N-WIci6TFjnOusSYPtM4o27o24jSrU68b8hRCA_AF_GqvY_PTZdzg_CPyTmleA</recordid><startdate>201812</startdate><enddate>201812</enddate><creator>Zhuang, Guang‐Chao</creator><creator>Peña‐Montenegro, Tito D.</creator><creator>Montgomery, Andrew</creator><creator>Hunter, Kimberley S.</creator><creator>Joye, Samantha B.</creator><general>John Wiley & Sons, Inc</general><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/0000-0003-1610-451X</orcidid><orcidid>https://orcid.org/0000-0002-2646-4183</orcidid><orcidid>https://orcid.org/0000-0002-6282-8415</orcidid></search><sort><creationdate>201812</creationdate><title>Microbial metabolism of methanol and methylamine in the Gulf of Mexico: insight into marine carbon and nitrogen cycling</title><author>Zhuang, Guang‐Chao ; Peña‐Montenegro, Tito D. ; Montgomery, Andrew ; Hunter, Kimberley S. ; Joye, Samantha B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3716-5551a78a9325466bf0a29b4cffce7a1b3b0b34f7fec2862c12b00d6b7457c15b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Ammonium</topic><topic>Ammonium compounds</topic><topic>Assimilation</topic><topic>Carbon</topic><topic>Carbon cycle</topic><topic>Carbon sources</topic><topic>Chlorophyll</topic><topic>Chlorophylls</topic><topic>Coastal waters</topic><topic>Dynamics</topic><topic>Metabolism</topic><topic>Methanol</topic><topic>Methylamine</topic><topic>Microorganisms</topic><topic>Mineral nutrients</topic><topic>Nitrogen</topic><topic>Nitrogen cycle</topic><topic>Nutrients</topic><topic>Offshore</topic><topic>Oxidation</topic><topic>Oxidation rate</topic><topic>Remineralization</topic><topic>Substrates</topic><topic>Surveying</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhuang, Guang‐Chao</creatorcontrib><creatorcontrib>Peña‐Montenegro, Tito D.</creatorcontrib><creatorcontrib>Montgomery, Andrew</creatorcontrib><creatorcontrib>Hunter, Kimberley S.</creatorcontrib><creatorcontrib>Joye, Samantha B.</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>Zhuang, Guang‐Chao</au><au>Peña‐Montenegro, Tito D.</au><au>Montgomery, Andrew</au><au>Hunter, Kimberley S.</au><au>Joye, Samantha B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microbial metabolism of methanol and methylamine in the Gulf of Mexico: insight into marine carbon and nitrogen cycling</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2018-12</date><risdate>2018</risdate><volume>20</volume><issue>12</issue><spage>4543</spage><epage>4554</epage><pages>4543-4554</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
One carbon (C1) metabolism plays an important role in marine carbon cycling but the dynamics and modes of C1 transformations are not fully understood. We made contemporaneous measurements of methylamine and methanol metabolism to elucidate the role of C1 compounds as sources of carbon, energy and nitrogen. Methanol and methylamine were predominantly used as an energy source in offshore waters (oxidation rate constant: kmethanol: 0.02−0.10 day−1; kmethylamine: 0.01−0.18 day−1), but were also important sources of biomass carbon in coastal waters (assimilation rate constant: kmethanol: 0.04−0.10 day−1; kmethylamine: 0.01−0.05 day−1). The relative extent of assimilation versus oxidation for these substrates correlated positively with chlorophyll, nutrients and heterotrophic bacterial production. Methanol oxidation and assimilation were stimulated significantly by nutrient addition. In contrast, methylamine metabolism was inhibited by ammonium or nitrate, suggesting that methylamine served as a nitrogen source. A preliminary metagenomic survey revealed a diverse population of putative C1‐utilizing microorganisms. These results show that the remineralization of methylamine could provide both C and N sources for microbes. Both methanol and methylamine contribute to microbial energetic and carbon substrate demands with a distinctly different signature in nearshore versus offshore environments.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>30209867</pmid><doi>10.1111/1462-2920.14406</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-1610-451X</orcidid><orcidid>https://orcid.org/0000-0002-2646-4183</orcidid><orcidid>https://orcid.org/0000-0002-6282-8415</orcidid></addata></record> |
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subjects | Ammonium Ammonium compounds Assimilation Carbon Carbon cycle Carbon sources Chlorophyll Chlorophylls Coastal waters Dynamics Metabolism Methanol Methylamine Microorganisms Mineral nutrients Nitrogen Nitrogen cycle Nutrients Offshore Oxidation Oxidation rate Remineralization Substrates Surveying |
title | Microbial metabolism of methanol and methylamine in the Gulf of Mexico: insight into marine carbon and nitrogen cycling |
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