Novel Alcaligenes ammonioxydans sp. nov. from wastewater treatment sludge oxidizes ammonia to N2 with a previously unknown pathway
Summary Heterotrophic nitrifiers are able to oxidize and remove ammonia from nitrogen‐rich wastewaters but the genetic elements of heterotrophic ammonia oxidation are poorly understood. Here, we isolated and identified a novel heterotrophic nitrifier, Alcaligenes ammonioxydans sp. nov. strain HO‐1,...
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| Veröffentlicht in: | Environmental microbiology 2021-11, Vol.23 (11), p.6965-6980 |
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| creator | Wu, Meng‐Ru Hou, Ting‐Ting Liu, Ying Miao, Li‐Li Ai, Guo‐Min Ma, Lan Zhu, Hai‐Zhen Zhu, Ya‐Xin Gao, Xi‐Yan Herbold, Craig W. Wagner, Michael Li, De‐Feng Liu, Zhi‐Pei Liu, Shuang‐Jiang |
| description | Summary
Heterotrophic nitrifiers are able to oxidize and remove ammonia from nitrogen‐rich wastewaters but the genetic elements of heterotrophic ammonia oxidation are poorly understood. Here, we isolated and identified a novel heterotrophic nitrifier, Alcaligenes ammonioxydans sp. nov. strain HO‐1, oxidizing ammonia to hydroxylamine and ending in the production of N2 gas. Genome analysis revealed that strain HO‐1 encoded a complete denitrification pathway but lacks any genes coding for homologous to known ammonia monooxygenases or hydroxylamine oxidoreductases. Our results demonstrated strain HO‐1 denitrified nitrite (not nitrate) to N2 and N2O at anaerobic and aerobic conditions respectively. Further experiments demonstrated that inhibition of aerobic denitrification did not stop ammonia oxidation and N2 production. A gene cluster (dnfT1RT2ABCD) was cloned from strain HO‐1 and enabled E. coli accumulated hydroxylamine. Sub‐cloning showed that genetic cluster dnfAB or dnfABC already enabled E. coli cells to produce hydroxylamine and further to 15N2 from (15NH4)2SO4. Transcriptome analysis revealed these three genes dnfA, dnfB and dnfC were significantly upregulated in response to ammonia stimulation. Taken together, we concluded that strain HO‐1 has a novel dnf genetic cluster for ammonia oxidation and this dnf genetic cluster encoded a previously unknown pathway of direct ammonia oxidation (Dirammox) to N2. |
| doi_str_mv | 10.1111/1462-2920.15751 |
| format | Article |
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Heterotrophic nitrifiers are able to oxidize and remove ammonia from nitrogen‐rich wastewaters but the genetic elements of heterotrophic ammonia oxidation are poorly understood. Here, we isolated and identified a novel heterotrophic nitrifier, Alcaligenes ammonioxydans sp. nov. strain HO‐1, oxidizing ammonia to hydroxylamine and ending in the production of N2 gas. Genome analysis revealed that strain HO‐1 encoded a complete denitrification pathway but lacks any genes coding for homologous to known ammonia monooxygenases or hydroxylamine oxidoreductases. Our results demonstrated strain HO‐1 denitrified nitrite (not nitrate) to N2 and N2O at anaerobic and aerobic conditions respectively. Further experiments demonstrated that inhibition of aerobic denitrification did not stop ammonia oxidation and N2 production. A gene cluster (dnfT1RT2ABCD) was cloned from strain HO‐1 and enabled E. coli accumulated hydroxylamine. Sub‐cloning showed that genetic cluster dnfAB or dnfABC already enabled E. coli cells to produce hydroxylamine and further to 15N2 from (15NH4)2SO4. Transcriptome analysis revealed these three genes dnfA, dnfB and dnfC were significantly upregulated in response to ammonia stimulation. Taken together, we concluded that strain HO‐1 has a novel dnf genetic cluster for ammonia oxidation and this dnf genetic cluster encoded a previously unknown pathway of direct ammonia oxidation (Dirammox) to N2.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.15751</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Aerobic conditions ; Alcaligenes ; Ammonia ; Anaerobic conditions ; Cloning ; Denitrification ; Dinitrofluorobenzene ; E coli ; Genes ; Genomes ; Homology ; Hydroxylamine ; Hydroxylamines ; New species ; Nitrous oxide ; Oxic conditions ; Oxidation ; Oxidoreductases ; Sludge ; Transcriptomes ; Wastewater treatment</subject><ispartof>Environmental microbiology, 2021-11, Vol.23 (11), p.6965-6980</ispartof><rights>2021 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2021 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0002-7585-310X ; 0000-0002-8683-019X</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%2F1462-2920.15751$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.15751$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids></links><search><creatorcontrib>Wu, Meng‐Ru</creatorcontrib><creatorcontrib>Hou, Ting‐Ting</creatorcontrib><creatorcontrib>Liu, Ying</creatorcontrib><creatorcontrib>Miao, Li‐Li</creatorcontrib><creatorcontrib>Ai, Guo‐Min</creatorcontrib><creatorcontrib>Ma, Lan</creatorcontrib><creatorcontrib>Zhu, Hai‐Zhen</creatorcontrib><creatorcontrib>Zhu, Ya‐Xin</creatorcontrib><creatorcontrib>Gao, Xi‐Yan</creatorcontrib><creatorcontrib>Herbold, Craig W.</creatorcontrib><creatorcontrib>Wagner, Michael</creatorcontrib><creatorcontrib>Li, De‐Feng</creatorcontrib><creatorcontrib>Liu, Zhi‐Pei</creatorcontrib><creatorcontrib>Liu, Shuang‐Jiang</creatorcontrib><title>Novel Alcaligenes ammonioxydans sp. nov. from wastewater treatment sludge oxidizes ammonia to N2 with a previously unknown pathway</title><title>Environmental microbiology</title><description>Summary
Heterotrophic nitrifiers are able to oxidize and remove ammonia from nitrogen‐rich wastewaters but the genetic elements of heterotrophic ammonia oxidation are poorly understood. Here, we isolated and identified a novel heterotrophic nitrifier, Alcaligenes ammonioxydans sp. nov. strain HO‐1, oxidizing ammonia to hydroxylamine and ending in the production of N2 gas. Genome analysis revealed that strain HO‐1 encoded a complete denitrification pathway but lacks any genes coding for homologous to known ammonia monooxygenases or hydroxylamine oxidoreductases. Our results demonstrated strain HO‐1 denitrified nitrite (not nitrate) to N2 and N2O at anaerobic and aerobic conditions respectively. Further experiments demonstrated that inhibition of aerobic denitrification did not stop ammonia oxidation and N2 production. A gene cluster (dnfT1RT2ABCD) was cloned from strain HO‐1 and enabled E. coli accumulated hydroxylamine. Sub‐cloning showed that genetic cluster dnfAB or dnfABC already enabled E. coli cells to produce hydroxylamine and further to 15N2 from (15NH4)2SO4. Transcriptome analysis revealed these three genes dnfA, dnfB and dnfC were significantly upregulated in response to ammonia stimulation. Taken together, we concluded that strain HO‐1 has a novel dnf genetic cluster for ammonia oxidation and this dnf genetic cluster encoded a previously unknown pathway of direct ammonia oxidation (Dirammox) to N2.</description><subject>Aerobic conditions</subject><subject>Alcaligenes</subject><subject>Ammonia</subject><subject>Anaerobic conditions</subject><subject>Cloning</subject><subject>Denitrification</subject><subject>Dinitrofluorobenzene</subject><subject>E coli</subject><subject>Genes</subject><subject>Genomes</subject><subject>Homology</subject><subject>Hydroxylamine</subject><subject>Hydroxylamines</subject><subject>New species</subject><subject>Nitrous oxide</subject><subject>Oxic conditions</subject><subject>Oxidation</subject><subject>Oxidoreductases</subject><subject>Sludge</subject><subject>Transcriptomes</subject><subject>Wastewater treatment</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNpdUT1PwzAQjRBIlI-Z1RILS4vtOI4zVlX5kPhYYLaO5AoGxw6x0xBGfjkpoA7ccPfu9PR0ei9JThidsbHOmZB8ygs-rlmesZ1ksr3sbjHj-8lBCK-UsjzN6ST5uvNrtGRuS7DmGR0GAnXtnfEfQwUukNDMiPPrGVm1viY9hIg9RGxJbBFijS6SYLvqGYn_MJX53AoAiZ7ccdKb-EKANC2uje-CHUjn3pzvHWkgvvQwHCV7K7ABj__mYfJ4sXxYXE1v7i-vF_ObacMlZ9OqAqFEJpkqQNFUUsyV4FLKjFJQWAgqS4ErTKV6UuWKMmClyHmJrMjoE0vTw-TsV7dp_XuHIerahBKtBYfjY5pneS4yNfaRevqP-uq71o3faS4pF1KleTGysl9WbywOumlNDe2gGdWbQPTGcr2xX_8Eope31z8g_QYRIIAr</recordid><startdate>202111</startdate><enddate>202111</enddate><creator>Wu, Meng‐Ru</creator><creator>Hou, Ting‐Ting</creator><creator>Liu, Ying</creator><creator>Miao, Li‐Li</creator><creator>Ai, Guo‐Min</creator><creator>Ma, Lan</creator><creator>Zhu, Hai‐Zhen</creator><creator>Zhu, Ya‐Xin</creator><creator>Gao, Xi‐Yan</creator><creator>Herbold, Craig W.</creator><creator>Wagner, Michael</creator><creator>Li, De‐Feng</creator><creator>Liu, Zhi‐Pei</creator><creator>Liu, Shuang‐Jiang</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><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/0000-0002-7585-310X</orcidid><orcidid>https://orcid.org/0000-0002-8683-019X</orcidid></search><sort><creationdate>202111</creationdate><title>Novel Alcaligenes ammonioxydans sp. nov. from wastewater treatment sludge oxidizes ammonia to N2 with a previously unknown pathway</title><author>Wu, Meng‐Ru ; Hou, Ting‐Ting ; Liu, Ying ; Miao, Li‐Li ; Ai, Guo‐Min ; Ma, Lan ; Zhu, Hai‐Zhen ; Zhu, Ya‐Xin ; Gao, Xi‐Yan ; Herbold, Craig W. ; Wagner, Michael ; Li, De‐Feng ; Liu, Zhi‐Pei ; Liu, Shuang‐Jiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p2621-dda48456189a80360e7842666500a8e9406c4efe368b8cf01a1c472ce1950b133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Aerobic conditions</topic><topic>Alcaligenes</topic><topic>Ammonia</topic><topic>Anaerobic conditions</topic><topic>Cloning</topic><topic>Denitrification</topic><topic>Dinitrofluorobenzene</topic><topic>E coli</topic><topic>Genes</topic><topic>Genomes</topic><topic>Homology</topic><topic>Hydroxylamine</topic><topic>Hydroxylamines</topic><topic>New species</topic><topic>Nitrous oxide</topic><topic>Oxic conditions</topic><topic>Oxidation</topic><topic>Oxidoreductases</topic><topic>Sludge</topic><topic>Transcriptomes</topic><topic>Wastewater treatment</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Meng‐Ru</creatorcontrib><creatorcontrib>Hou, Ting‐Ting</creatorcontrib><creatorcontrib>Liu, Ying</creatorcontrib><creatorcontrib>Miao, Li‐Li</creatorcontrib><creatorcontrib>Ai, Guo‐Min</creatorcontrib><creatorcontrib>Ma, Lan</creatorcontrib><creatorcontrib>Zhu, Hai‐Zhen</creatorcontrib><creatorcontrib>Zhu, Ya‐Xin</creatorcontrib><creatorcontrib>Gao, Xi‐Yan</creatorcontrib><creatorcontrib>Herbold, Craig W.</creatorcontrib><creatorcontrib>Wagner, Michael</creatorcontrib><creatorcontrib>Li, De‐Feng</creatorcontrib><creatorcontrib>Liu, Zhi‐Pei</creatorcontrib><creatorcontrib>Liu, Shuang‐Jiang</creatorcontrib><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>Wu, Meng‐Ru</au><au>Hou, Ting‐Ting</au><au>Liu, Ying</au><au>Miao, Li‐Li</au><au>Ai, Guo‐Min</au><au>Ma, Lan</au><au>Zhu, Hai‐Zhen</au><au>Zhu, Ya‐Xin</au><au>Gao, Xi‐Yan</au><au>Herbold, Craig W.</au><au>Wagner, Michael</au><au>Li, De‐Feng</au><au>Liu, Zhi‐Pei</au><au>Liu, Shuang‐Jiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Novel Alcaligenes ammonioxydans sp. nov. from wastewater treatment sludge oxidizes ammonia to N2 with a previously unknown pathway</atitle><jtitle>Environmental microbiology</jtitle><date>2021-11</date><risdate>2021</risdate><volume>23</volume><issue>11</issue><spage>6965</spage><epage>6980</epage><pages>6965-6980</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Heterotrophic nitrifiers are able to oxidize and remove ammonia from nitrogen‐rich wastewaters but the genetic elements of heterotrophic ammonia oxidation are poorly understood. Here, we isolated and identified a novel heterotrophic nitrifier, Alcaligenes ammonioxydans sp. nov. strain HO‐1, oxidizing ammonia to hydroxylamine and ending in the production of N2 gas. Genome analysis revealed that strain HO‐1 encoded a complete denitrification pathway but lacks any genes coding for homologous to known ammonia monooxygenases or hydroxylamine oxidoreductases. Our results demonstrated strain HO‐1 denitrified nitrite (not nitrate) to N2 and N2O at anaerobic and aerobic conditions respectively. Further experiments demonstrated that inhibition of aerobic denitrification did not stop ammonia oxidation and N2 production. A gene cluster (dnfT1RT2ABCD) was cloned from strain HO‐1 and enabled E. coli accumulated hydroxylamine. Sub‐cloning showed that genetic cluster dnfAB or dnfABC already enabled E. coli cells to produce hydroxylamine and further to 15N2 from (15NH4)2SO4. Transcriptome analysis revealed these three genes dnfA, dnfB and dnfC were significantly upregulated in response to ammonia stimulation. Taken together, we concluded that strain HO‐1 has a novel dnf genetic cluster for ammonia oxidation and this dnf genetic cluster encoded a previously unknown pathway of direct ammonia oxidation (Dirammox) to N2.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><doi>10.1111/1462-2920.15751</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-7585-310X</orcidid><orcidid>https://orcid.org/0000-0002-8683-019X</orcidid></addata></record> |
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| source | Wiley Online Library Journals Frontfile Complete |
| subjects | Aerobic conditions Alcaligenes Ammonia Anaerobic conditions Cloning Denitrification Dinitrofluorobenzene E coli Genes Genomes Homology Hydroxylamine Hydroxylamines New species Nitrous oxide Oxic conditions Oxidation Oxidoreductases Sludge Transcriptomes Wastewater treatment |
| title | Novel Alcaligenes ammonioxydans sp. nov. from wastewater treatment sludge oxidizes ammonia to N2 with a previously unknown pathway |
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