Mimicking microbial interactions under nitrate‐reducing conditions in an anoxic bioreactor: enrichment of novel Nitrospirae bacteria distantly related to Thermodesulfovibrio
Summary Microorganisms are main drivers of the sulfur, nitrogen and carbon biogeochemical cycles. These elemental cycles are interconnected by the activity of different guilds in sediments or wastewater treatment systems. Here, we investigated a nitrate‐reducing microbial community in a laboratory‐s...
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| Veröffentlicht in: | Environmental microbiology 2017-12, Vol.19 (12), p.4965-4977 |
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| creator | Arshad, Arslan Dalcin Martins, Paula Frank, Jeroen Jetten, Mike S. M. Op den Camp, Huub J. M. Welte, Cornelia U. |
| description | Summary
Microorganisms are main drivers of the sulfur, nitrogen and carbon biogeochemical cycles. These elemental cycles are interconnected by the activity of different guilds in sediments or wastewater treatment systems. Here, we investigated a nitrate‐reducing microbial community in a laboratory‐scale bioreactor model that closely mimicked estuary or brackish sediment conditions. The bioreactor simultaneously consumed sulfide, methane and ammonium at the expense of nitrate. Ammonium oxidation occurred solely by the activity of anammox bacteria identified as Candidatus Scalindua brodae and Ca. Kuenenia stuttgartiensis. Fifty‐three percent of methane oxidation was catalyzed by archaea affiliated to Ca. Methanoperedens and 47% by Ca. Methylomirabilis bacteria. Sulfide oxidation was mainly shared between two proteobacterial groups. Interestingly, competition for nitrate did not lead to exclusion of one particular group. Metagenomic analysis showed that the most abundant taxonomic group was distantly related to Thermodesulfovibrio sp. (87–89% 16S rRNA gene identity, 52–54% average amino acid identity), representing a new family within the Nitrospirae phylum. A high quality draft genome of the new species was recovered, and analysis showed high metabolic versatility. Related microbial groups are found in diverse environments with sulfur, nitrogen and methane cycling, indicating that these novel Nitrospirae bacteria might contribute to biogeochemical cycling in natural habitats. |
| doi_str_mv | 10.1111/1462-2920.13977 |
| format | Article |
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Microorganisms are main drivers of the sulfur, nitrogen and carbon biogeochemical cycles. These elemental cycles are interconnected by the activity of different guilds in sediments or wastewater treatment systems. Here, we investigated a nitrate‐reducing microbial community in a laboratory‐scale bioreactor model that closely mimicked estuary or brackish sediment conditions. The bioreactor simultaneously consumed sulfide, methane and ammonium at the expense of nitrate. Ammonium oxidation occurred solely by the activity of anammox bacteria identified as Candidatus Scalindua brodae and Ca. Kuenenia stuttgartiensis. Fifty‐three percent of methane oxidation was catalyzed by archaea affiliated to Ca. Methanoperedens and 47% by Ca. Methylomirabilis bacteria. Sulfide oxidation was mainly shared between two proteobacterial groups. Interestingly, competition for nitrate did not lead to exclusion of one particular group. Metagenomic analysis showed that the most abundant taxonomic group was distantly related to Thermodesulfovibrio sp. (87–89% 16S rRNA gene identity, 52–54% average amino acid identity), representing a new family within the Nitrospirae phylum. A high quality draft genome of the new species was recovered, and analysis showed high metabolic versatility. Related microbial groups are found in diverse environments with sulfur, nitrogen and methane cycling, indicating that these novel Nitrospirae bacteria might contribute to biogeochemical cycling in natural habitats.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.13977</identifier><identifier>PMID: 29105249</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Amino Acid Sequence ; Amino acids ; Ammonia-oxidizing bacteria ; Ammonium ; Ammonium compounds ; Ammonium Compounds - metabolism ; Anoxia ; Anoxic sediments ; Archaea ; Archaea - genetics ; Archaea - metabolism ; Bacteria ; Bacteria - classification ; Bacteria - genetics ; Bacteria - metabolism ; Biogeochemical cycle ; Biogeochemical cycles ; Biogeochemistry ; Bioreactors ; Bioreactors - microbiology ; Candidatus Kuenenia stuttgartiensis ; Candidatus Methanoperedens ; Candidatus Methylomirabilis ; Candidatus Scalindua ; Carbon cycle ; Cycles ; Estuaries ; Estuarine dynamics ; Estuarine environments ; Genomes ; Guilds ; Interactions ; Methane ; Methane - metabolism ; Microbial Interactions ; Microorganisms ; Mimicry ; New family ; New species ; Nitrates ; Nitrates - metabolism ; Nitrites - metabolism ; Nitrogen ; Nitrospira ; Oxidation ; Oxidation-Reduction ; Phylogeny ; RNA, Ribosomal, 16S - genetics ; rRNA 16S ; Sediments ; Sulfide ; Sulfides ; Sulfides - metabolism ; Sulfur ; Sulphides ; Sulphur ; Thermodesulfobacteria ; Wastewater ; Wastewater treatment</subject><ispartof>Environmental microbiology, 2017-12, Vol.19 (12), p.4965-4977</ispartof><rights>2017 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2017 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4127-777777f3dbeb13e4af3eff5b1cde6aa46bdcea2f46df357a42eeaf61858220973</citedby><cites>FETCH-LOGICAL-c4127-777777f3dbeb13e4af3eff5b1cde6aa46bdcea2f46df357a42eeaf61858220973</cites><orcidid>0000-0002-1568-8878</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%2F1462-2920.13977$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.13977$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29105249$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Arshad, Arslan</creatorcontrib><creatorcontrib>Dalcin Martins, Paula</creatorcontrib><creatorcontrib>Frank, Jeroen</creatorcontrib><creatorcontrib>Jetten, Mike S. M.</creatorcontrib><creatorcontrib>Op den Camp, Huub J. M.</creatorcontrib><creatorcontrib>Welte, Cornelia U.</creatorcontrib><title>Mimicking microbial interactions under nitrate‐reducing conditions in an anoxic bioreactor: enrichment of novel Nitrospirae bacteria distantly related to Thermodesulfovibrio</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Microorganisms are main drivers of the sulfur, nitrogen and carbon biogeochemical cycles. These elemental cycles are interconnected by the activity of different guilds in sediments or wastewater treatment systems. Here, we investigated a nitrate‐reducing microbial community in a laboratory‐scale bioreactor model that closely mimicked estuary or brackish sediment conditions. The bioreactor simultaneously consumed sulfide, methane and ammonium at the expense of nitrate. Ammonium oxidation occurred solely by the activity of anammox bacteria identified as Candidatus Scalindua brodae and Ca. Kuenenia stuttgartiensis. Fifty‐three percent of methane oxidation was catalyzed by archaea affiliated to Ca. Methanoperedens and 47% by Ca. Methylomirabilis bacteria. Sulfide oxidation was mainly shared between two proteobacterial groups. Interestingly, competition for nitrate did not lead to exclusion of one particular group. Metagenomic analysis showed that the most abundant taxonomic group was distantly related to Thermodesulfovibrio sp. (87–89% 16S rRNA gene identity, 52–54% average amino acid identity), representing a new family within the Nitrospirae phylum. A high quality draft genome of the new species was recovered, and analysis showed high metabolic versatility. Related microbial groups are found in diverse environments with sulfur, nitrogen and methane cycling, indicating that these novel Nitrospirae bacteria might contribute to biogeochemical cycling in natural habitats.</description><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Ammonia-oxidizing bacteria</subject><subject>Ammonium</subject><subject>Ammonium compounds</subject><subject>Ammonium Compounds - metabolism</subject><subject>Anoxia</subject><subject>Anoxic sediments</subject><subject>Archaea</subject><subject>Archaea - genetics</subject><subject>Archaea - metabolism</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Biogeochemical cycle</subject><subject>Biogeochemical cycles</subject><subject>Biogeochemistry</subject><subject>Bioreactors</subject><subject>Bioreactors - microbiology</subject><subject>Candidatus Kuenenia stuttgartiensis</subject><subject>Candidatus Methanoperedens</subject><subject>Candidatus Methylomirabilis</subject><subject>Candidatus Scalindua</subject><subject>Carbon cycle</subject><subject>Cycles</subject><subject>Estuaries</subject><subject>Estuarine dynamics</subject><subject>Estuarine environments</subject><subject>Genomes</subject><subject>Guilds</subject><subject>Interactions</subject><subject>Methane</subject><subject>Methane - metabolism</subject><subject>Microbial Interactions</subject><subject>Microorganisms</subject><subject>Mimicry</subject><subject>New family</subject><subject>New species</subject><subject>Nitrates</subject><subject>Nitrates - metabolism</subject><subject>Nitrites - metabolism</subject><subject>Nitrogen</subject><subject>Nitrospira</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>Phylogeny</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>rRNA 16S</subject><subject>Sediments</subject><subject>Sulfide</subject><subject>Sulfides</subject><subject>Sulfides - metabolism</subject><subject>Sulfur</subject><subject>Sulphides</subject><subject>Sulphur</subject><subject>Thermodesulfobacteria</subject><subject>Wastewater</subject><subject>Wastewater treatment</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkbtuFTEQhi0EIiFQ0yFLNDSH2N6Ld-lQFCBSAk2oV76MyQSvfbB3E07HI_AmvBNPgjcbTkHDyNJ4Rt_8Hvkn5Dlnr3mJY163YiN6Ucqql_IBOdx3Hu7vXByQJzlfM8ZlJdljclB6rBF1f0h-XeCI5iuGL7TkFDUqTzFMkJSZMIZM52Ah0YBTUhP8_vEzgZ3NwpsYLK4MBqqWE7-joRpjgjId0xsKIaG5GiFMNDoa4g14-rFIxbzFpIDqwkFCRS3mSYXJ72gCXx6ydIr08grSGC3k2bt4gzphfEoeOeUzPLvPR-Tzu9PLkw-b80_vz07enm9MzYXcyLtwldWgeQW1chU412huLLRK1a22BpRwdWtd1UhVCwDlWt41nRCsl9URebXqblP8NkOehhGzAe9VgDjngfctZ5UUXV3Ql_-g13FOoWxXKNnxpmM9K9TxSpVPzjmBG7YJR5V2A2fD4uWwuDUszg13XpaJF_e6sx7B7vm_5hWgWYFb9LD7n95wenG2Cv8BaZKvdQ</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Arshad, Arslan</creator><creator>Dalcin Martins, Paula</creator><creator>Frank, Jeroen</creator><creator>Jetten, Mike S. M.</creator><creator>Op den Camp, Huub J. M.</creator><creator>Welte, Cornelia U.</creator><general>Wiley Subscription Services, Inc</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>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/0000-0002-1568-8878</orcidid></search><sort><creationdate>201712</creationdate><title>Mimicking microbial interactions under nitrate‐reducing conditions in an anoxic bioreactor: enrichment of novel Nitrospirae bacteria distantly related to Thermodesulfovibrio</title><author>Arshad, Arslan ; Dalcin Martins, Paula ; Frank, Jeroen ; Jetten, Mike S. M. ; Op den Camp, Huub J. M. ; Welte, Cornelia U.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4127-777777f3dbeb13e4af3eff5b1cde6aa46bdcea2f46df357a42eeaf61858220973</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Amino Acid Sequence</topic><topic>Amino acids</topic><topic>Ammonia-oxidizing bacteria</topic><topic>Ammonium</topic><topic>Ammonium compounds</topic><topic>Ammonium Compounds - metabolism</topic><topic>Anoxia</topic><topic>Anoxic sediments</topic><topic>Archaea</topic><topic>Archaea - genetics</topic><topic>Archaea - metabolism</topic><topic>Bacteria</topic><topic>Bacteria - classification</topic><topic>Bacteria - genetics</topic><topic>Bacteria - metabolism</topic><topic>Biogeochemical cycle</topic><topic>Biogeochemical cycles</topic><topic>Biogeochemistry</topic><topic>Bioreactors</topic><topic>Bioreactors - microbiology</topic><topic>Candidatus Kuenenia stuttgartiensis</topic><topic>Candidatus Methanoperedens</topic><topic>Candidatus Methylomirabilis</topic><topic>Candidatus Scalindua</topic><topic>Carbon cycle</topic><topic>Cycles</topic><topic>Estuaries</topic><topic>Estuarine dynamics</topic><topic>Estuarine environments</topic><topic>Genomes</topic><topic>Guilds</topic><topic>Interactions</topic><topic>Methane</topic><topic>Methane - metabolism</topic><topic>Microbial Interactions</topic><topic>Microorganisms</topic><topic>Mimicry</topic><topic>New family</topic><topic>New species</topic><topic>Nitrates</topic><topic>Nitrates - metabolism</topic><topic>Nitrites - metabolism</topic><topic>Nitrogen</topic><topic>Nitrospira</topic><topic>Oxidation</topic><topic>Oxidation-Reduction</topic><topic>Phylogeny</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>rRNA 16S</topic><topic>Sediments</topic><topic>Sulfide</topic><topic>Sulfides</topic><topic>Sulfides - metabolism</topic><topic>Sulfur</topic><topic>Sulphides</topic><topic>Sulphur</topic><topic>Thermodesulfobacteria</topic><topic>Wastewater</topic><topic>Wastewater treatment</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Arshad, Arslan</creatorcontrib><creatorcontrib>Dalcin Martins, Paula</creatorcontrib><creatorcontrib>Frank, Jeroen</creatorcontrib><creatorcontrib>Jetten, Mike S. 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M.</creatorcontrib><creatorcontrib>Welte, Cornelia U.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><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>Arshad, Arslan</au><au>Dalcin Martins, Paula</au><au>Frank, Jeroen</au><au>Jetten, Mike S. M.</au><au>Op den Camp, Huub J. M.</au><au>Welte, Cornelia U.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mimicking microbial interactions under nitrate‐reducing conditions in an anoxic bioreactor: enrichment of novel Nitrospirae bacteria distantly related to Thermodesulfovibrio</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2017-12</date><risdate>2017</risdate><volume>19</volume><issue>12</issue><spage>4965</spage><epage>4977</epage><pages>4965-4977</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Microorganisms are main drivers of the sulfur, nitrogen and carbon biogeochemical cycles. These elemental cycles are interconnected by the activity of different guilds in sediments or wastewater treatment systems. Here, we investigated a nitrate‐reducing microbial community in a laboratory‐scale bioreactor model that closely mimicked estuary or brackish sediment conditions. The bioreactor simultaneously consumed sulfide, methane and ammonium at the expense of nitrate. Ammonium oxidation occurred solely by the activity of anammox bacteria identified as Candidatus Scalindua brodae and Ca. Kuenenia stuttgartiensis. Fifty‐three percent of methane oxidation was catalyzed by archaea affiliated to Ca. Methanoperedens and 47% by Ca. Methylomirabilis bacteria. Sulfide oxidation was mainly shared between two proteobacterial groups. Interestingly, competition for nitrate did not lead to exclusion of one particular group. Metagenomic analysis showed that the most abundant taxonomic group was distantly related to Thermodesulfovibrio sp. (87–89% 16S rRNA gene identity, 52–54% average amino acid identity), representing a new family within the Nitrospirae phylum. A high quality draft genome of the new species was recovered, and analysis showed high metabolic versatility. Related microbial groups are found in diverse environments with sulfur, nitrogen and methane cycling, indicating that these novel Nitrospirae bacteria might contribute to biogeochemical cycling in natural habitats.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>29105249</pmid><doi>10.1111/1462-2920.13977</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-1568-8878</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Environmental microbiology, 2017-12, Vol.19 (12), p.4965-4977 |
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| subjects | Amino Acid Sequence Amino acids Ammonia-oxidizing bacteria Ammonium Ammonium compounds Ammonium Compounds - metabolism Anoxia Anoxic sediments Archaea Archaea - genetics Archaea - metabolism Bacteria Bacteria - classification Bacteria - genetics Bacteria - metabolism Biogeochemical cycle Biogeochemical cycles Biogeochemistry Bioreactors Bioreactors - microbiology Candidatus Kuenenia stuttgartiensis Candidatus Methanoperedens Candidatus Methylomirabilis Candidatus Scalindua Carbon cycle Cycles Estuaries Estuarine dynamics Estuarine environments Genomes Guilds Interactions Methane Methane - metabolism Microbial Interactions Microorganisms Mimicry New family New species Nitrates Nitrates - metabolism Nitrites - metabolism Nitrogen Nitrospira Oxidation Oxidation-Reduction Phylogeny RNA, Ribosomal, 16S - genetics rRNA 16S Sediments Sulfide Sulfides Sulfides - metabolism Sulfur Sulphides Sulphur Thermodesulfobacteria Wastewater Wastewater treatment |
| title | Mimicking microbial interactions under nitrate‐reducing conditions in an anoxic bioreactor: enrichment of novel Nitrospirae bacteria distantly related to Thermodesulfovibrio |
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