Complete nitrification by a single microorganism
Until now, the oxidation steps necessary for complete nitrification had always been observed to occur in two separate microorganisms in a cross-feeding interaction; here, together with the study by Daims et al ., van Kessel et al . report the enrichment and characterization of Nitrospira species tha...
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description | Until now, the oxidation steps necessary for complete nitrification had always been observed to occur in two separate microorganisms in a cross-feeding interaction; here, together with the study by Daims
et al
., van Kessel
et al
. report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as ‘comammox’ (for complete ammonia oxidation).
Time to rethink nitrification
Two groups this week report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as 'comammox' (for complete ammonia oxidation). Until now, this two-step reaction was thought to involve two organisms in a cross-feeding interaction. Phylogenetic analyses suggest that comammox
Nitrospira
are present in a number of diverse environments, so these findings have the potential to fundamentally change our view of the nitrogen cycle and open a new frontier in nitrification research.
Nitrification is a two-step process where ammonia is first oxidized to nitrite by ammonia-oxidizing bacteria and/or archaea, and subsequently to nitrate by nitrite-oxidizing bacteria. Already described by Winogradsky in 1890
1
, this division of labour between the two functional groups is a generally accepted characteristic of the biogeochemical nitrogen cycle
2
. Complete oxidation of ammonia to nitrate in one organism (complete ammonia oxidation; comammox) is energetically feasible, and it was postulated that this process could occur under conditions selecting for species with lower growth rates but higher growth yields than canonical ammonia-oxidizing microorganisms
3
. Still, organisms catalysing this process have not yet been discovered. Here we report the enrichment and initial characterization of two
Nitrospira
species that encode all the enzymes necessary for ammonia oxidation via nitrite to nitrate in their genomes, and indeed completely oxidize ammonium to nitrate to conserve energy. Their ammonia monooxygenase (AMO) enzymes are phylogenetically distinct from currently identified AMOs, rendering recent acquisition by horizontal gene transfer from known ammonia-oxidizing microorganisms unlikely. We also found highly similar
amoA
sequences (encoding the AMO subunit A) in public sequence databases, which were apparently misclassified as methane monooxygenases. This recognition of a novel
amoA
sequence group w |
doi_str_mv | 10.1038/nature16459 |
format | Article |
fullrecord | <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4878690</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A438950305</galeid><sourcerecordid>A438950305</sourcerecordid><originalsourceid>FETCH-LOGICAL-c715t-1b01bce6561dd25307a23c2459ad7de66bab443af26b09aca40857451dd9a25f3</originalsourceid><addsrcrecordid>eNpt0t9r1TAUB_AgDnedPvkuxb0orjNpkzR5EcZF3WAg-OM5pOlpzWiTuyQV99-by53z3lH6EOj55Ns05yD0iuBzgmvxwek0ByCcMvkErQhteEm5aJ6iFcaVKLGo-TF6HuMNxpiRhj5DxxXnJBfZCuG1nzYjJCicTcH21uhkvSvau0IX0bphhGKyJngfBu1snF6go16PEV7eryfo5-dPP9aX5fXXL1fri-vSNISlkrSYtAY446TrKlbjRle1qfIZddd0wHmrW0pr3Ve8xVIbTbFgDWVZS12xvj5BH3e5m7mdoDPgUtCj2gQ76XCnvLbqsOLsLzX434qKRnCJc8Db-4Dgb2eISU02GhhH7cDPUZGGESkkYTTT00f0xs_B5d_bqopIIiX5rwY9grKu9_m7ZhuqLmgtJMM1ZlmVC2oAB_mQ3kFv8-sD_2bBm429VfvofAHlp4PcnMXUdwcbsknwJw16jlFdff92aN_vbO5yjAH6h0smWG0nTO1NWNav9_vyYP-NVAZnOxBzyQ0Q9i5zIe8vbA3Xzw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1752191991</pqid></control><display><type>article</type><title>Complete nitrification by a single microorganism</title><source>MEDLINE</source><source>Springer Nature - Complete Springer Journals</source><source>Nature Journals Online</source><creator>van Kessel, Maartje A. H. J. ; Speth, Daan R. ; Albertsen, Mads ; Nielsen, Per H. ; Op den Camp, Huub J. M. ; Kartal, Boran ; Jetten, Mike S. M. ; Lücker, Sebastian</creator><creatorcontrib>van Kessel, Maartje A. H. J. ; Speth, Daan R. ; Albertsen, Mads ; Nielsen, Per H. ; Op den Camp, Huub J. M. ; Kartal, Boran ; Jetten, Mike S. M. ; Lücker, Sebastian</creatorcontrib><description>Until now, the oxidation steps necessary for complete nitrification had always been observed to occur in two separate microorganisms in a cross-feeding interaction; here, together with the study by Daims
et al
., van Kessel
et al
. report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as ‘comammox’ (for complete ammonia oxidation).
Time to rethink nitrification
Two groups this week report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as 'comammox' (for complete ammonia oxidation). Until now, this two-step reaction was thought to involve two organisms in a cross-feeding interaction. Phylogenetic analyses suggest that comammox
Nitrospira
are present in a number of diverse environments, so these findings have the potential to fundamentally change our view of the nitrogen cycle and open a new frontier in nitrification research.
Nitrification is a two-step process where ammonia is first oxidized to nitrite by ammonia-oxidizing bacteria and/or archaea, and subsequently to nitrate by nitrite-oxidizing bacteria. Already described by Winogradsky in 1890
1
, this division of labour between the two functional groups is a generally accepted characteristic of the biogeochemical nitrogen cycle
2
. Complete oxidation of ammonia to nitrate in one organism (complete ammonia oxidation; comammox) is energetically feasible, and it was postulated that this process could occur under conditions selecting for species with lower growth rates but higher growth yields than canonical ammonia-oxidizing microorganisms
3
. Still, organisms catalysing this process have not yet been discovered. Here we report the enrichment and initial characterization of two
Nitrospira
species that encode all the enzymes necessary for ammonia oxidation via nitrite to nitrate in their genomes, and indeed completely oxidize ammonium to nitrate to conserve energy. Their ammonia monooxygenase (AMO) enzymes are phylogenetically distinct from currently identified AMOs, rendering recent acquisition by horizontal gene transfer from known ammonia-oxidizing microorganisms unlikely. We also found highly similar
amoA
sequences (encoding the AMO subunit A) in public sequence databases, which were apparently misclassified as methane monooxygenases. This recognition of a novel
amoA
sequence group will lead to an improved understanding of the environmental abundance and distribution of ammonia-oxidizing microorganisms. Furthermore, the discovery of the long-sought-after comammox process will change our perception of the nitrogen cycle.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature16459</identifier><identifier>PMID: 26610025</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/326/171/1818 ; 631/326/171/1878 ; 631/326/41/1969 ; 631/326/41/2142 ; Ammonia ; Ammonia - metabolism ; Ammonium ; Bacteria ; Bacteria - enzymology ; Bacteria - genetics ; Bacteria - metabolism ; Bacteria, Nitrifying ; Biogeochemical cycles ; Biogeochemistry ; Biosynthesis ; Cytochrome ; Energy conservation ; Enzymes ; Evolution, Molecular ; Genes ; Genome, Bacterial - genetics ; Genomes ; Humanities and Social Sciences ; letter ; Microorganisms ; multidisciplinary ; Nitrates ; Nitrates - metabolism ; Nitrification ; Nitrification - genetics ; Nitrites - metabolism ; Nitrogen cycle ; Observations ; Organisms ; Oxidation ; Oxidation-Reduction ; Oxidoreductases - genetics ; Oxidoreductases - metabolism ; Phylogenetics ; Phylogeny ; Physiological aspects ; Proteins ; Science ; Soil microbiology</subject><ispartof>Nature (London), 2015-12, Vol.528 (7583), p.555-559</ispartof><rights>Springer Nature Limited 2015</rights><rights>COPYRIGHT 2015 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Dec 24-Dec 31, 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c715t-1b01bce6561dd25307a23c2459ad7de66bab443af26b09aca40857451dd9a25f3</citedby><cites>FETCH-LOGICAL-c715t-1b01bce6561dd25307a23c2459ad7de66bab443af26b09aca40857451dd9a25f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature16459$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature16459$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,777,781,882,27905,27906,41469,42538,51300</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26610025$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>van Kessel, Maartje A. H. J.</creatorcontrib><creatorcontrib>Speth, Daan R.</creatorcontrib><creatorcontrib>Albertsen, Mads</creatorcontrib><creatorcontrib>Nielsen, Per H.</creatorcontrib><creatorcontrib>Op den Camp, Huub J. M.</creatorcontrib><creatorcontrib>Kartal, Boran</creatorcontrib><creatorcontrib>Jetten, Mike S. M.</creatorcontrib><creatorcontrib>Lücker, Sebastian</creatorcontrib><title>Complete nitrification by a single microorganism</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Until now, the oxidation steps necessary for complete nitrification had always been observed to occur in two separate microorganisms in a cross-feeding interaction; here, together with the study by Daims
et al
., van Kessel
et al
. report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as ‘comammox’ (for complete ammonia oxidation).
Time to rethink nitrification
Two groups this week report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as 'comammox' (for complete ammonia oxidation). Until now, this two-step reaction was thought to involve two organisms in a cross-feeding interaction. Phylogenetic analyses suggest that comammox
Nitrospira
are present in a number of diverse environments, so these findings have the potential to fundamentally change our view of the nitrogen cycle and open a new frontier in nitrification research.
Nitrification is a two-step process where ammonia is first oxidized to nitrite by ammonia-oxidizing bacteria and/or archaea, and subsequently to nitrate by nitrite-oxidizing bacteria. Already described by Winogradsky in 1890
1
, this division of labour between the two functional groups is a generally accepted characteristic of the biogeochemical nitrogen cycle
2
. Complete oxidation of ammonia to nitrate in one organism (complete ammonia oxidation; comammox) is energetically feasible, and it was postulated that this process could occur under conditions selecting for species with lower growth rates but higher growth yields than canonical ammonia-oxidizing microorganisms
3
. Still, organisms catalysing this process have not yet been discovered. Here we report the enrichment and initial characterization of two
Nitrospira
species that encode all the enzymes necessary for ammonia oxidation via nitrite to nitrate in their genomes, and indeed completely oxidize ammonium to nitrate to conserve energy. Their ammonia monooxygenase (AMO) enzymes are phylogenetically distinct from currently identified AMOs, rendering recent acquisition by horizontal gene transfer from known ammonia-oxidizing microorganisms unlikely. We also found highly similar
amoA
sequences (encoding the AMO subunit A) in public sequence databases, which were apparently misclassified as methane monooxygenases. This recognition of a novel
amoA
sequence group will lead to an improved understanding of the environmental abundance and distribution of ammonia-oxidizing microorganisms. Furthermore, the discovery of the long-sought-after comammox process will change our perception of the nitrogen cycle.</description><subject>631/326/171/1818</subject><subject>631/326/171/1878</subject><subject>631/326/41/1969</subject><subject>631/326/41/2142</subject><subject>Ammonia</subject><subject>Ammonia - metabolism</subject><subject>Ammonium</subject><subject>Bacteria</subject><subject>Bacteria - enzymology</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Bacteria, Nitrifying</subject><subject>Biogeochemical cycles</subject><subject>Biogeochemistry</subject><subject>Biosynthesis</subject><subject>Cytochrome</subject><subject>Energy conservation</subject><subject>Enzymes</subject><subject>Evolution, Molecular</subject><subject>Genes</subject><subject>Genome, Bacterial - genetics</subject><subject>Genomes</subject><subject>Humanities and Social Sciences</subject><subject>letter</subject><subject>Microorganisms</subject><subject>multidisciplinary</subject><subject>Nitrates</subject><subject>Nitrates - metabolism</subject><subject>Nitrification</subject><subject>Nitrification - genetics</subject><subject>Nitrites - metabolism</subject><subject>Nitrogen cycle</subject><subject>Observations</subject><subject>Organisms</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>Oxidoreductases - genetics</subject><subject>Oxidoreductases - metabolism</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Science</subject><subject>Soil microbiology</subject><issn>0028-0836</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpt0t9r1TAUB_AgDnedPvkuxb0orjNpkzR5EcZF3WAg-OM5pOlpzWiTuyQV99-by53z3lH6EOj55Ns05yD0iuBzgmvxwek0ByCcMvkErQhteEm5aJ6iFcaVKLGo-TF6HuMNxpiRhj5DxxXnJBfZCuG1nzYjJCicTcH21uhkvSvau0IX0bphhGKyJngfBu1snF6go16PEV7eryfo5-dPP9aX5fXXL1fri-vSNISlkrSYtAY446TrKlbjRle1qfIZddd0wHmrW0pr3Ve8xVIbTbFgDWVZS12xvj5BH3e5m7mdoDPgUtCj2gQ76XCnvLbqsOLsLzX434qKRnCJc8Db-4Dgb2eISU02GhhH7cDPUZGGESkkYTTT00f0xs_B5d_bqopIIiX5rwY9grKu9_m7ZhuqLmgtJMM1ZlmVC2oAB_mQ3kFv8-sD_2bBm429VfvofAHlp4PcnMXUdwcbsknwJw16jlFdff92aN_vbO5yjAH6h0smWG0nTO1NWNav9_vyYP-NVAZnOxBzyQ0Q9i5zIe8vbA3Xzw</recordid><startdate>20151224</startdate><enddate>20151224</enddate><creator>van Kessel, Maartje A. 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H. J. ; Speth, Daan R. ; Albertsen, Mads ; Nielsen, Per H. ; Op den Camp, Huub J. M. ; Kartal, Boran ; Jetten, Mike S. M. ; Lücker, Sebastian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c715t-1b01bce6561dd25307a23c2459ad7de66bab443af26b09aca40857451dd9a25f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>631/326/171/1818</topic><topic>631/326/171/1878</topic><topic>631/326/41/1969</topic><topic>631/326/41/2142</topic><topic>Ammonia</topic><topic>Ammonia - metabolism</topic><topic>Ammonium</topic><topic>Bacteria</topic><topic>Bacteria - enzymology</topic><topic>Bacteria - genetics</topic><topic>Bacteria - metabolism</topic><topic>Bacteria, Nitrifying</topic><topic>Biogeochemical cycles</topic><topic>Biogeochemistry</topic><topic>Biosynthesis</topic><topic>Cytochrome</topic><topic>Energy conservation</topic><topic>Enzymes</topic><topic>Evolution, Molecular</topic><topic>Genes</topic><topic>Genome, Bacterial - genetics</topic><topic>Genomes</topic><topic>Humanities and Social Sciences</topic><topic>letter</topic><topic>Microorganisms</topic><topic>multidisciplinary</topic><topic>Nitrates</topic><topic>Nitrates - metabolism</topic><topic>Nitrification</topic><topic>Nitrification - genetics</topic><topic>Nitrites - metabolism</topic><topic>Nitrogen cycle</topic><topic>Observations</topic><topic>Organisms</topic><topic>Oxidation</topic><topic>Oxidation-Reduction</topic><topic>Oxidoreductases - genetics</topic><topic>Oxidoreductases - metabolism</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Science</topic><topic>Soil microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>van Kessel, Maartje A. H. J.</creatorcontrib><creatorcontrib>Speth, Daan R.</creatorcontrib><creatorcontrib>Albertsen, Mads</creatorcontrib><creatorcontrib>Nielsen, Per H.</creatorcontrib><creatorcontrib>Op den Camp, Huub J. M.</creatorcontrib><creatorcontrib>Kartal, Boran</creatorcontrib><creatorcontrib>Jetten, Mike S. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>van Kessel, Maartje A. H. J.</au><au>Speth, Daan R.</au><au>Albertsen, Mads</au><au>Nielsen, Per H.</au><au>Op den Camp, Huub J. M.</au><au>Kartal, Boran</au><au>Jetten, Mike S. M.</au><au>Lücker, Sebastian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Complete nitrification by a single microorganism</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2015-12-24</date><risdate>2015</risdate><volume>528</volume><issue>7583</issue><spage>555</spage><epage>559</epage><pages>555-559</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><coden>NATUAS</coden><abstract>Until now, the oxidation steps necessary for complete nitrification had always been observed to occur in two separate microorganisms in a cross-feeding interaction; here, together with the study by Daims
et al
., van Kessel
et al
. report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as ‘comammox’ (for complete ammonia oxidation).
Time to rethink nitrification
Two groups this week report the enrichment and characterization of
Nitrospira
species that encode all of the enzymes necessary to catalyse complete nitrification, a phenotype referred to as 'comammox' (for complete ammonia oxidation). Until now, this two-step reaction was thought to involve two organisms in a cross-feeding interaction. Phylogenetic analyses suggest that comammox
Nitrospira
are present in a number of diverse environments, so these findings have the potential to fundamentally change our view of the nitrogen cycle and open a new frontier in nitrification research.
Nitrification is a two-step process where ammonia is first oxidized to nitrite by ammonia-oxidizing bacteria and/or archaea, and subsequently to nitrate by nitrite-oxidizing bacteria. Already described by Winogradsky in 1890
1
, this division of labour between the two functional groups is a generally accepted characteristic of the biogeochemical nitrogen cycle
2
. Complete oxidation of ammonia to nitrate in one organism (complete ammonia oxidation; comammox) is energetically feasible, and it was postulated that this process could occur under conditions selecting for species with lower growth rates but higher growth yields than canonical ammonia-oxidizing microorganisms
3
. Still, organisms catalysing this process have not yet been discovered. Here we report the enrichment and initial characterization of two
Nitrospira
species that encode all the enzymes necessary for ammonia oxidation via nitrite to nitrate in their genomes, and indeed completely oxidize ammonium to nitrate to conserve energy. Their ammonia monooxygenase (AMO) enzymes are phylogenetically distinct from currently identified AMOs, rendering recent acquisition by horizontal gene transfer from known ammonia-oxidizing microorganisms unlikely. We also found highly similar
amoA
sequences (encoding the AMO subunit A) in public sequence databases, which were apparently misclassified as methane monooxygenases. This recognition of a novel
amoA
sequence group will lead to an improved understanding of the environmental abundance and distribution of ammonia-oxidizing microorganisms. Furthermore, the discovery of the long-sought-after comammox process will change our perception of the nitrogen cycle.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>26610025</pmid><doi>10.1038/nature16459</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0028-0836 |
ispartof | Nature (London), 2015-12, Vol.528 (7583), p.555-559 |
issn | 0028-0836 1476-4687 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4878690 |
source | MEDLINE; Springer Nature - Complete Springer Journals; Nature Journals Online |
subjects | 631/326/171/1818 631/326/171/1878 631/326/41/1969 631/326/41/2142 Ammonia Ammonia - metabolism Ammonium Bacteria Bacteria - enzymology Bacteria - genetics Bacteria - metabolism Bacteria, Nitrifying Biogeochemical cycles Biogeochemistry Biosynthesis Cytochrome Energy conservation Enzymes Evolution, Molecular Genes Genome, Bacterial - genetics Genomes Humanities and Social Sciences letter Microorganisms multidisciplinary Nitrates Nitrates - metabolism Nitrification Nitrification - genetics Nitrites - metabolism Nitrogen cycle Observations Organisms Oxidation Oxidation-Reduction Oxidoreductases - genetics Oxidoreductases - metabolism Phylogenetics Phylogeny Physiological aspects Proteins Science Soil microbiology |
title | Complete nitrification by a single microorganism |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-19T17%3A19%3A26IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Complete%20nitrification%20by%20a%20single%20microorganism&rft.jtitle=Nature%20(London)&rft.au=van%20Kessel,%20Maartje%20A.%20H.%20J.&rft.date=2015-12-24&rft.volume=528&rft.issue=7583&rft.spage=555&rft.epage=559&rft.pages=555-559&rft.issn=0028-0836&rft.eissn=1476-4687&rft.coden=NATUAS&rft_id=info:doi/10.1038/nature16459&rft_dat=%3Cgale_pubme%3EA438950305%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1752191991&rft_id=info:pmid/26610025&rft_galeid=A438950305&rfr_iscdi=true |