Metabolic activity analyses demonstrate that Lokiarchaeon exhibits homoacetogenesis in sulfidic marine sediments
The genomes of the Asgard superphylum of Archaea hold clues pertaining to the nature of the host cell that acquired the mitochondrion at the origin of eukaryotes 1 – 4 . Representatives of the Asgard candidate phylum Candidatus Lokiarchaeota (Lokiarchaeon) have the capacity for acetogenesis and ferm...
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| Veröffentlicht in: | Nature microbiology 2020-02, Vol.5 (2), p.248-255 |
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| creator | Orsi, William D. Vuillemin, Aurèle Rodriguez, Paula Coskun, Ömer K. Gomez-Saez, Gonzalo V. Lavik, Gaute Mohrholz, Volker Ferdelman, Timothy G. |
| description | The genomes of the Asgard superphylum of Archaea hold clues pertaining to the nature of the host cell that acquired the mitochondrion at the origin of eukaryotes
1
–
4
. Representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota (Lokiarchaeon) have the capacity for acetogenesis and fermentation
5
–
7
, but how their metabolic activity responds to environmental conditions is poorly understood. Here, we show that in anoxic Namibian shelf sediments, Lokiarchaeon gene expression levels are higher than those of bacterial phyla and increase with depth below the seafloor. Lokiarchaeon gene expression was significantly different across a hypoxic–sulfidic redox gradient, whereby genes involved in growth, fermentation and H
2
-dependent carbon fixation had the highest expression under the most reducing (sulfidic) conditions. Quantitative stable isotope probing revealed that anaerobic utilization of CO
2
and diatomaceous extracellular polymeric substances by Lokiarchaeon was higher than the bacterial average, consistent with higher expression of Lokiarchaeon genes, including those involved in transport and fermentation of sugars and amino acids. The quantitative stable isotope probing and gene expression data demonstrate homoacetogenic activity of
Candidatus
Lokiarchaeota, whereby fermentative H
2
production from organic substrates is coupled with the Wood–Ljungdahl carbon fixation pathway
8
. The high energetic efficiency provided by homoacetogenesis
8
helps to explain the elevated metabolic activity of Lokiarchaeon in this anoxic, energy-limited setting.
Quantitative stable isotope probing and gene expression analyses in anoxic Namibian shelf sediments reveal that representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota are capable of homoacetogenesis, a metabolic strategy of high energetic efficiency that may explain how these archaea thrive in the energy-limited seafloor subsurface environment. |
| doi_str_mv | 10.1038/s41564-019-0630-3 |
| format | Article |
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1
–
4
. Representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota (Lokiarchaeon) have the capacity for acetogenesis and fermentation
5
–
7
, but how their metabolic activity responds to environmental conditions is poorly understood. Here, we show that in anoxic Namibian shelf sediments, Lokiarchaeon gene expression levels are higher than those of bacterial phyla and increase with depth below the seafloor. Lokiarchaeon gene expression was significantly different across a hypoxic–sulfidic redox gradient, whereby genes involved in growth, fermentation and H
2
-dependent carbon fixation had the highest expression under the most reducing (sulfidic) conditions. Quantitative stable isotope probing revealed that anaerobic utilization of CO
2
and diatomaceous extracellular polymeric substances by Lokiarchaeon was higher than the bacterial average, consistent with higher expression of Lokiarchaeon genes, including those involved in transport and fermentation of sugars and amino acids. The quantitative stable isotope probing and gene expression data demonstrate homoacetogenic activity of
Candidatus
Lokiarchaeota, whereby fermentative H
2
production from organic substrates is coupled with the Wood–Ljungdahl carbon fixation pathway
8
. The high energetic efficiency provided by homoacetogenesis
8
helps to explain the elevated metabolic activity of Lokiarchaeon in this anoxic, energy-limited setting.
Quantitative stable isotope probing and gene expression analyses in anoxic Namibian shelf sediments reveal that representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota are capable of homoacetogenesis, a metabolic strategy of high energetic efficiency that may explain how these archaea thrive in the energy-limited seafloor subsurface environment.</description><identifier>ISSN: 2058-5276</identifier><identifier>EISSN: 2058-5276</identifier><identifier>DOI: 10.1038/s41564-019-0630-3</identifier><identifier>PMID: 31873205</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/22 ; 38/23 ; 38/39 ; 38/47 ; 38/71 ; 38/77 ; 38/90 ; 38/91 ; 45/29 ; 631/158/855 ; 631/326/26/2527 ; 704/47 ; Acetogenesis ; Anaerobiosis ; Archaea ; Archaea - classification ; Archaea - genetics ; Archaea - metabolism ; Biomedical and Life Sciences ; Candidatus Lokiarchaeota ; Carbon Cycle ; Carbon dioxide ; Carbon fixation ; Energy Metabolism ; Environmental conditions ; Fermentation ; Gene expression ; Genome, Archaeal ; Genomes ; Geologic Sediments - microbiology ; Homoacetogenesis ; Hypoxia ; Infectious Diseases ; Letter ; Life Sciences ; Medical Microbiology ; Metabolism ; Metagenomics ; Microbiology ; Models, Biological ; Ocean floor ; Oxidation-Reduction ; Parasitology ; Sediments ; Sulfides - metabolism ; Virology</subject><ispartof>Nature microbiology, 2020-02, Vol.5 (2), p.248-255</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2019</rights><rights>The Author(s), under exclusive licence to Springer Nature Limited 2019.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c400t-6de8392d24ef55ac55d78bf2a3a03211c32f2b5ecea6c88a6ddb7903e1a54fc83</citedby><cites>FETCH-LOGICAL-c400t-6de8392d24ef55ac55d78bf2a3a03211c32f2b5ecea6c88a6ddb7903e1a54fc83</cites><orcidid>0000-0002-7724-8931 ; 0000-0003-0778-9182 ; 0000-0002-9701-3793 ; 0000-0002-4094-5637</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41564-019-0630-3$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41564-019-0630-3$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31873205$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Orsi, William D.</creatorcontrib><creatorcontrib>Vuillemin, Aurèle</creatorcontrib><creatorcontrib>Rodriguez, Paula</creatorcontrib><creatorcontrib>Coskun, Ömer K.</creatorcontrib><creatorcontrib>Gomez-Saez, Gonzalo V.</creatorcontrib><creatorcontrib>Lavik, Gaute</creatorcontrib><creatorcontrib>Mohrholz, Volker</creatorcontrib><creatorcontrib>Ferdelman, Timothy G.</creatorcontrib><title>Metabolic activity analyses demonstrate that Lokiarchaeon exhibits homoacetogenesis in sulfidic marine sediments</title><title>Nature microbiology</title><addtitle>Nat Microbiol</addtitle><addtitle>Nat Microbiol</addtitle><description>The genomes of the Asgard superphylum of Archaea hold clues pertaining to the nature of the host cell that acquired the mitochondrion at the origin of eukaryotes
1
–
4
. Representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota (Lokiarchaeon) have the capacity for acetogenesis and fermentation
5
–
7
, but how their metabolic activity responds to environmental conditions is poorly understood. Here, we show that in anoxic Namibian shelf sediments, Lokiarchaeon gene expression levels are higher than those of bacterial phyla and increase with depth below the seafloor. Lokiarchaeon gene expression was significantly different across a hypoxic–sulfidic redox gradient, whereby genes involved in growth, fermentation and H
2
-dependent carbon fixation had the highest expression under the most reducing (sulfidic) conditions. Quantitative stable isotope probing revealed that anaerobic utilization of CO
2
and diatomaceous extracellular polymeric substances by Lokiarchaeon was higher than the bacterial average, consistent with higher expression of Lokiarchaeon genes, including those involved in transport and fermentation of sugars and amino acids. The quantitative stable isotope probing and gene expression data demonstrate homoacetogenic activity of
Candidatus
Lokiarchaeota, whereby fermentative H
2
production from organic substrates is coupled with the Wood–Ljungdahl carbon fixation pathway
8
. The high energetic efficiency provided by homoacetogenesis
8
helps to explain the elevated metabolic activity of Lokiarchaeon in this anoxic, energy-limited setting.
Quantitative stable isotope probing and gene expression analyses in anoxic Namibian shelf sediments reveal that representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota are capable of homoacetogenesis, a metabolic strategy of high energetic efficiency that may explain how these archaea thrive in the energy-limited seafloor subsurface environment.</description><subject>38/22</subject><subject>38/23</subject><subject>38/39</subject><subject>38/47</subject><subject>38/71</subject><subject>38/77</subject><subject>38/90</subject><subject>38/91</subject><subject>45/29</subject><subject>631/158/855</subject><subject>631/326/26/2527</subject><subject>704/47</subject><subject>Acetogenesis</subject><subject>Anaerobiosis</subject><subject>Archaea</subject><subject>Archaea - classification</subject><subject>Archaea - genetics</subject><subject>Archaea - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Candidatus Lokiarchaeota</subject><subject>Carbon Cycle</subject><subject>Carbon dioxide</subject><subject>Carbon fixation</subject><subject>Energy Metabolism</subject><subject>Environmental conditions</subject><subject>Fermentation</subject><subject>Gene expression</subject><subject>Genome, Archaeal</subject><subject>Genomes</subject><subject>Geologic Sediments - microbiology</subject><subject>Homoacetogenesis</subject><subject>Hypoxia</subject><subject>Infectious Diseases</subject><subject>Letter</subject><subject>Life Sciences</subject><subject>Medical Microbiology</subject><subject>Metabolism</subject><subject>Metagenomics</subject><subject>Microbiology</subject><subject>Models, Biological</subject><subject>Ocean floor</subject><subject>Oxidation-Reduction</subject><subject>Parasitology</subject><subject>Sediments</subject><subject>Sulfides - metabolism</subject><subject>Virology</subject><issn>2058-5276</issn><issn>2058-5276</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kU1rFDEYgIMottT-AC8S8OJlNN-TPUqxWljxoueQSd7pps4k67wZ6f57s2z9QNBcEsiTJ_A-hDzn7DVn0r5BxbVRHeObjhnJOvmInAumbadFbx7_cT4jl4h3jDFuhDHWPCVnktteNuCc7D9C9UOZUqA-1PQ91QP12U8HBKQR5pKxLr4CrTtf6bZ8TX4JOw8lU7jfpSFVpLsyFx-gllvIgAlpyhTXaUyxWWe_pAwUIaYZcsVn5MnoJ4TLh_2CfLl-9_nqQ7f99P7m6u22C4qx2pkIVm5EFApGrX3QOvZ2GIWXnknBeZBiFIOGAN4Ea72Jceg3TAL3Wo3Bygvy6uTdL-XbCljdnDDANPkMZUUnpGSyLaUb-vIv9K6sSxtCo1SvmbJWy_9SUvVKSc5Uo_iJCktBXGB0-yW1GRwcZ-7YzZ26udbNHbu5o_nFg3kdZoi_Xvys1ABxArBd5VtYfn_9b-sP8fSkEQ</recordid><startdate>20200201</startdate><enddate>20200201</enddate><creator>Orsi, William D.</creator><creator>Vuillemin, Aurèle</creator><creator>Rodriguez, Paula</creator><creator>Coskun, Ömer K.</creator><creator>Gomez-Saez, Gonzalo V.</creator><creator>Lavik, Gaute</creator><creator>Mohrholz, Volker</creator><creator>Ferdelman, Timothy G.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>8FE</scope><scope>8FH</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7724-8931</orcidid><orcidid>https://orcid.org/0000-0003-0778-9182</orcidid><orcidid>https://orcid.org/0000-0002-9701-3793</orcidid><orcidid>https://orcid.org/0000-0002-4094-5637</orcidid></search><sort><creationdate>20200201</creationdate><title>Metabolic activity analyses demonstrate that Lokiarchaeon exhibits homoacetogenesis in sulfidic marine sediments</title><author>Orsi, William D. ; Vuillemin, Aurèle ; Rodriguez, Paula ; Coskun, Ömer K. ; Gomez-Saez, Gonzalo V. ; Lavik, Gaute ; Mohrholz, Volker ; Ferdelman, Timothy G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c400t-6de8392d24ef55ac55d78bf2a3a03211c32f2b5ecea6c88a6ddb7903e1a54fc83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>38/22</topic><topic>38/23</topic><topic>38/39</topic><topic>38/47</topic><topic>38/71</topic><topic>38/77</topic><topic>38/90</topic><topic>38/91</topic><topic>45/29</topic><topic>631/158/855</topic><topic>631/326/26/2527</topic><topic>704/47</topic><topic>Acetogenesis</topic><topic>Anaerobiosis</topic><topic>Archaea</topic><topic>Archaea - classification</topic><topic>Archaea - genetics</topic><topic>Archaea - metabolism</topic><topic>Biomedical and Life Sciences</topic><topic>Candidatus Lokiarchaeota</topic><topic>Carbon Cycle</topic><topic>Carbon dioxide</topic><topic>Carbon fixation</topic><topic>Energy Metabolism</topic><topic>Environmental conditions</topic><topic>Fermentation</topic><topic>Gene expression</topic><topic>Genome, Archaeal</topic><topic>Genomes</topic><topic>Geologic Sediments - microbiology</topic><topic>Homoacetogenesis</topic><topic>Hypoxia</topic><topic>Infectious Diseases</topic><topic>Letter</topic><topic>Life Sciences</topic><topic>Medical Microbiology</topic><topic>Metabolism</topic><topic>Metagenomics</topic><topic>Microbiology</topic><topic>Models, Biological</topic><topic>Ocean floor</topic><topic>Oxidation-Reduction</topic><topic>Parasitology</topic><topic>Sediments</topic><topic>Sulfides - metabolism</topic><topic>Virology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Orsi, William D.</creatorcontrib><creatorcontrib>Vuillemin, Aurèle</creatorcontrib><creatorcontrib>Rodriguez, Paula</creatorcontrib><creatorcontrib>Coskun, Ömer K.</creatorcontrib><creatorcontrib>Gomez-Saez, Gonzalo V.</creatorcontrib><creatorcontrib>Lavik, Gaute</creatorcontrib><creatorcontrib>Mohrholz, Volker</creatorcontrib><creatorcontrib>Ferdelman, Timothy G.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>ProQuest Biological Science Journals</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><jtitle>Nature microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Orsi, William D.</au><au>Vuillemin, Aurèle</au><au>Rodriguez, Paula</au><au>Coskun, Ömer K.</au><au>Gomez-Saez, Gonzalo V.</au><au>Lavik, Gaute</au><au>Mohrholz, Volker</au><au>Ferdelman, Timothy G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metabolic activity analyses demonstrate that Lokiarchaeon exhibits homoacetogenesis in sulfidic marine sediments</atitle><jtitle>Nature microbiology</jtitle><stitle>Nat Microbiol</stitle><addtitle>Nat Microbiol</addtitle><date>2020-02-01</date><risdate>2020</risdate><volume>5</volume><issue>2</issue><spage>248</spage><epage>255</epage><pages>248-255</pages><issn>2058-5276</issn><eissn>2058-5276</eissn><abstract>The genomes of the Asgard superphylum of Archaea hold clues pertaining to the nature of the host cell that acquired the mitochondrion at the origin of eukaryotes
1
–
4
. Representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota (Lokiarchaeon) have the capacity for acetogenesis and fermentation
5
–
7
, but how their metabolic activity responds to environmental conditions is poorly understood. Here, we show that in anoxic Namibian shelf sediments, Lokiarchaeon gene expression levels are higher than those of bacterial phyla and increase with depth below the seafloor. Lokiarchaeon gene expression was significantly different across a hypoxic–sulfidic redox gradient, whereby genes involved in growth, fermentation and H
2
-dependent carbon fixation had the highest expression under the most reducing (sulfidic) conditions. Quantitative stable isotope probing revealed that anaerobic utilization of CO
2
and diatomaceous extracellular polymeric substances by Lokiarchaeon was higher than the bacterial average, consistent with higher expression of Lokiarchaeon genes, including those involved in transport and fermentation of sugars and amino acids. The quantitative stable isotope probing and gene expression data demonstrate homoacetogenic activity of
Candidatus
Lokiarchaeota, whereby fermentative H
2
production from organic substrates is coupled with the Wood–Ljungdahl carbon fixation pathway
8
. The high energetic efficiency provided by homoacetogenesis
8
helps to explain the elevated metabolic activity of Lokiarchaeon in this anoxic, energy-limited setting.
Quantitative stable isotope probing and gene expression analyses in anoxic Namibian shelf sediments reveal that representatives of the Asgard candidate phylum
Candidatus
Lokiarchaeota are capable of homoacetogenesis, a metabolic strategy of high energetic efficiency that may explain how these archaea thrive in the energy-limited seafloor subsurface environment.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31873205</pmid><doi>10.1038/s41564-019-0630-3</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-7724-8931</orcidid><orcidid>https://orcid.org/0000-0003-0778-9182</orcidid><orcidid>https://orcid.org/0000-0002-9701-3793</orcidid><orcidid>https://orcid.org/0000-0002-4094-5637</orcidid></addata></record> |
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| subjects | 38/22 38/23 38/39 38/47 38/71 38/77 38/90 38/91 45/29 631/158/855 631/326/26/2527 704/47 Acetogenesis Anaerobiosis Archaea Archaea - classification Archaea - genetics Archaea - metabolism Biomedical and Life Sciences Candidatus Lokiarchaeota Carbon Cycle Carbon dioxide Carbon fixation Energy Metabolism Environmental conditions Fermentation Gene expression Genome, Archaeal Genomes Geologic Sediments - microbiology Homoacetogenesis Hypoxia Infectious Diseases Letter Life Sciences Medical Microbiology Metabolism Metagenomics Microbiology Models, Biological Ocean floor Oxidation-Reduction Parasitology Sediments Sulfides - metabolism Virology |
| title | Metabolic activity analyses demonstrate that Lokiarchaeon exhibits homoacetogenesis in sulfidic marine sediments |
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