Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin
Copper plays a critical role in controlling greenhouse gas emissions as it is a key component of the particulate methane monooxygenase and nitrous oxide reductase. Some methanotrophs excrete methanobactin (MB) that has an extremely high copper affinity. As a result, MB may limit the ability of other...
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| Veröffentlicht in: | Environmental microbiology 2023-11, Vol.25 (11), p.2338-2350 |
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| creator | Chang, Jin Peng, Peng Farhan Ul‐Haque, Muhammad Hira, Abid DiSpirito, Alan A. Semrau, Jeremy D. |
| description | Copper plays a critical role in controlling greenhouse gas emissions as it is a key component of the particulate methane monooxygenase and nitrous oxide reductase. Some methanotrophs excrete methanobactin (MB) that has an extremely high copper affinity. As a result, MB may limit the ability of other microbes to gather copper, thereby decreasing their activity as well as impacting microbial community composition. Here, we show using forest soil microcosms that multiple forms of MB; MB from Methylosinus trichosporium OB3b (MB‐OB3b) and MB from Methylocystis sp. strain SB2 (MB‐SB2) increased nitrous oxide (N2O) production as well caused significant shifts in microbial community composition. Such effects, however, were mediated by the amount of copper in the soils, with low‐copper soil microcosms showing the strongest response to MB. Furthermore, MB‐SB2 had a stronger effect, likely due to its higher affinity for copper. The presence of either form of MB also inhibited nitrite reduction and generally increased the presence of genes encoding for the iron‐containing nitrite reductase (nirS) over the copper‐dependent nitrite reductase (nirK). These data indicate the methanotrophic‐mediated production of MB can significantly impact multiple steps of denitrification, as well as have broad effects on microbial community composition of forest soils. |
| doi_str_mv | 10.1111/1462-2920.16456 |
| format | Article |
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Some methanotrophs excrete methanobactin (MB) that has an extremely high copper affinity. As a result, MB may limit the ability of other microbes to gather copper, thereby decreasing their activity as well as impacting microbial community composition. Here, we show using forest soil microcosms that multiple forms of MB; MB from Methylosinus trichosporium OB3b (MB‐OB3b) and MB from Methylocystis sp. strain SB2 (MB‐SB2) increased nitrous oxide (N2O) production as well caused significant shifts in microbial community composition. Such effects, however, were mediated by the amount of copper in the soils, with low‐copper soil microcosms showing the strongest response to MB. Furthermore, MB‐SB2 had a stronger effect, likely due to its higher affinity for copper. The presence of either form of MB also inhibited nitrite reduction and generally increased the presence of genes encoding for the iron‐containing nitrite reductase (nirS) over the copper‐dependent nitrite reductase (nirK). These data indicate the methanotrophic‐mediated production of MB can significantly impact multiple steps of denitrification, as well as have broad effects on microbial community composition of forest soils.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.16456</identifier><identifier>PMID: 37395163</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>60 APPLIED LIFE SCIENCES ; Affinity ; BASIC BIOLOGICAL SCIENCES ; biogenic global cycles ; Community composition ; Composition effects ; Copper ; Denitrification ; Emissions ; ENVIRONMENTAL SCIENCES ; Forest soils ; Genes ; Greenhouse gases ; metals ; Methane monooxygenase ; Methanotrophic bacteria ; microbial communities ; microbially-influenced global change ; Microbiomes ; Microcosms ; Microorganisms ; NirK protein ; Nitrite reductase ; Nitrites ; Nitrous oxide ; Reductases ; Reduction ; Soil ; soil microbes ; Soils</subject><ispartof>Environmental microbiology, 2023-11, Vol.25 (11), p.2338-2350</ispartof><rights>2023 Applied Microbiology International and John Wiley & Sons Ltd.</rights><rights>2023 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3936-3eec2ce871aed79615c6a8e8044a14777d08cd1140487acabb7dca5c5691339b3</cites><orcidid>0000-0002-0584-8874 ; 0000-0002-1670-9984 ; 0000000205848874 ; 0000000216709984</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%2F1462-2920.16456$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.16456$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37395163$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1991190$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Chang, Jin</creatorcontrib><creatorcontrib>Peng, Peng</creatorcontrib><creatorcontrib>Farhan Ul‐Haque, Muhammad</creatorcontrib><creatorcontrib>Hira, Abid</creatorcontrib><creatorcontrib>DiSpirito, Alan A.</creatorcontrib><creatorcontrib>Semrau, Jeremy D.</creatorcontrib><creatorcontrib>Univ. of Michigan, Ann Arbor, MI (United States)</creatorcontrib><title>Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Copper plays a critical role in controlling greenhouse gas emissions as it is a key component of the particulate methane monooxygenase and nitrous oxide reductase. Some methanotrophs excrete methanobactin (MB) that has an extremely high copper affinity. As a result, MB may limit the ability of other microbes to gather copper, thereby decreasing their activity as well as impacting microbial community composition. Here, we show using forest soil microcosms that multiple forms of MB; MB from Methylosinus trichosporium OB3b (MB‐OB3b) and MB from Methylocystis sp. strain SB2 (MB‐SB2) increased nitrous oxide (N2O) production as well caused significant shifts in microbial community composition. Such effects, however, were mediated by the amount of copper in the soils, with low‐copper soil microcosms showing the strongest response to MB. Furthermore, MB‐SB2 had a stronger effect, likely due to its higher affinity for copper. The presence of either form of MB also inhibited nitrite reduction and generally increased the presence of genes encoding for the iron‐containing nitrite reductase (nirS) over the copper‐dependent nitrite reductase (nirK). These data indicate the methanotrophic‐mediated production of MB can significantly impact multiple steps of denitrification, as well as have broad effects on microbial community composition of forest soils.</description><subject>60 APPLIED LIFE SCIENCES</subject><subject>Affinity</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>biogenic global cycles</subject><subject>Community composition</subject><subject>Composition effects</subject><subject>Copper</subject><subject>Denitrification</subject><subject>Emissions</subject><subject>ENVIRONMENTAL SCIENCES</subject><subject>Forest soils</subject><subject>Genes</subject><subject>Greenhouse gases</subject><subject>metals</subject><subject>Methane monooxygenase</subject><subject>Methanotrophic bacteria</subject><subject>microbial communities</subject><subject>microbially-influenced global change</subject><subject>Microbiomes</subject><subject>Microcosms</subject><subject>Microorganisms</subject><subject>NirK protein</subject><subject>Nitrite reductase</subject><subject>Nitrites</subject><subject>Nitrous oxide</subject><subject>Reductases</subject><subject>Reduction</subject><subject>Soil</subject><subject>soil microbes</subject><subject>Soils</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNqFkUFv1DAQhS0EoqVw5oYseullqSdOYvuIqrasVMSlPVuOM9G6SuxiJ4L998w2ZQ9c8MWe8TfPen6MfQTxBWhdQt1Wm8pUVLZ1075ip8fO6-MZqhP2rpRHIUBJJd6yE6mkaaCVp8xv4y50YQ4p8jTwGOaclsLT79Ajz9gv_vkqRD6kjGXmJYWRT8Hn5FOZCu_2vA_DgBnjfGCoRToTzjsXU-doPL5nbwY3Fvzwsp-xh5vr-6tvm7sft9urr3cbL41sNxLRVx61Aoe9Mi00vnUatahrB7VSqhfa9wC1qLVy3nWd6r1rfNMakNJ08ox9XnVTmYMtPszodz7FiH62YAyAEQRdrNBTTj8XcmSnUDyOo4tIzm2lZaXpiQYIPf8HfUxLjmSBKG1qDQQTdblS9CWlZBzsUw6Ty3sLwh5CsocY7CES-xwSTXx60V26Cfsj_zcVApoV-BVG3P9Pz15_367CfwB_6Jtp</recordid><startdate>202311</startdate><enddate>202311</enddate><creator>Chang, Jin</creator><creator>Peng, Peng</creator><creator>Farhan Ul‐Haque, Muhammad</creator><creator>Hira, Abid</creator><creator>DiSpirito, Alan A.</creator><creator>Semrau, Jeremy D.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><general>Wiley</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><scope>OIOZB</scope><scope>OTOTI</scope><orcidid>https://orcid.org/0000-0002-0584-8874</orcidid><orcidid>https://orcid.org/0000-0002-1670-9984</orcidid><orcidid>https://orcid.org/0000000205848874</orcidid><orcidid>https://orcid.org/0000000216709984</orcidid></search><sort><creationdate>202311</creationdate><title>Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin</title><author>Chang, Jin ; Peng, Peng ; Farhan Ul‐Haque, Muhammad ; Hira, Abid ; DiSpirito, Alan A. ; Semrau, Jeremy D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3936-3eec2ce871aed79615c6a8e8044a14777d08cd1140487acabb7dca5c5691339b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>60 APPLIED LIFE SCIENCES</topic><topic>Affinity</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>biogenic global cycles</topic><topic>Community composition</topic><topic>Composition effects</topic><topic>Copper</topic><topic>Denitrification</topic><topic>Emissions</topic><topic>ENVIRONMENTAL SCIENCES</topic><topic>Forest soils</topic><topic>Genes</topic><topic>Greenhouse gases</topic><topic>metals</topic><topic>Methane monooxygenase</topic><topic>Methanotrophic bacteria</topic><topic>microbial communities</topic><topic>microbially-influenced global change</topic><topic>Microbiomes</topic><topic>Microcosms</topic><topic>Microorganisms</topic><topic>NirK protein</topic><topic>Nitrite reductase</topic><topic>Nitrites</topic><topic>Nitrous oxide</topic><topic>Reductases</topic><topic>Reduction</topic><topic>Soil</topic><topic>soil microbes</topic><topic>Soils</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chang, Jin</creatorcontrib><creatorcontrib>Peng, Peng</creatorcontrib><creatorcontrib>Farhan Ul‐Haque, Muhammad</creatorcontrib><creatorcontrib>Hira, Abid</creatorcontrib><creatorcontrib>DiSpirito, Alan A.</creatorcontrib><creatorcontrib>Semrau, Jeremy D.</creatorcontrib><creatorcontrib>Univ. of Michigan, Ann Arbor, MI (United States)</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><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chang, Jin</au><au>Peng, Peng</au><au>Farhan Ul‐Haque, Muhammad</au><au>Hira, Abid</au><au>DiSpirito, Alan A.</au><au>Semrau, Jeremy D.</au><aucorp>Univ. of Michigan, Ann Arbor, MI (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2023-11</date><risdate>2023</risdate><volume>25</volume><issue>11</issue><spage>2338</spage><epage>2350</epage><pages>2338-2350</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Copper plays a critical role in controlling greenhouse gas emissions as it is a key component of the particulate methane monooxygenase and nitrous oxide reductase. Some methanotrophs excrete methanobactin (MB) that has an extremely high copper affinity. As a result, MB may limit the ability of other microbes to gather copper, thereby decreasing their activity as well as impacting microbial community composition. Here, we show using forest soil microcosms that multiple forms of MB; MB from Methylosinus trichosporium OB3b (MB‐OB3b) and MB from Methylocystis sp. strain SB2 (MB‐SB2) increased nitrous oxide (N2O) production as well caused significant shifts in microbial community composition. Such effects, however, were mediated by the amount of copper in the soils, with low‐copper soil microcosms showing the strongest response to MB. Furthermore, MB‐SB2 had a stronger effect, likely due to its higher affinity for copper. The presence of either form of MB also inhibited nitrite reduction and generally increased the presence of genes encoding for the iron‐containing nitrite reductase (nirS) over the copper‐dependent nitrite reductase (nirK). These data indicate the methanotrophic‐mediated production of MB can significantly impact multiple steps of denitrification, as well as have broad effects on microbial community composition of forest soils.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>37395163</pmid><doi>10.1111/1462-2920.16456</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-0584-8874</orcidid><orcidid>https://orcid.org/0000-0002-1670-9984</orcidid><orcidid>https://orcid.org/0000000205848874</orcidid><orcidid>https://orcid.org/0000000216709984</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Wiley Online Library Journals Frontfile Complete |
| subjects | 60 APPLIED LIFE SCIENCES Affinity BASIC BIOLOGICAL SCIENCES biogenic global cycles Community composition Composition effects Copper Denitrification Emissions ENVIRONMENTAL SCIENCES Forest soils Genes Greenhouse gases metals Methane monooxygenase Methanotrophic bacteria microbial communities microbially-influenced global change Microbiomes Microcosms Microorganisms NirK protein Nitrite reductase Nitrites Nitrous oxide Reductases Reduction Soil soil microbes Soils |
| title | Inhibition of nitrous oxide reduction in forest soil microcosms by different forms of methanobactin |
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