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Metabolic dependencies govern microbial syntrophies during methanogenesis in an anaerobic digestion ecosystem
Methanogenesis, a biological process mediated by complex microbial communities, has attracted great attention due to its contribution to global warming and potential in biotechnological applications. The current study unveiled the core microbial methanogenic metabolisms in anaerobic vessel ecosystem...
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Published in: | Microbiome 2020-02, Vol.8 (1), p.22-14, Article 22 |
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description | Methanogenesis, a biological process mediated by complex microbial communities, has attracted great attention due to its contribution to global warming and potential in biotechnological applications. The current study unveiled the core microbial methanogenic metabolisms in anaerobic vessel ecosystems by applying combined genome-centric metagenomics and metatranscriptomics. Here, we demonstrate that an enriched natural system, fueled only with acetate, could support a bacteria-dominated microbiota employing a multi-trophic methanogenic process. Moreover, significant changes, in terms of microbial structure and function, were recorded after the system was supplemented with additional H
. Methanosarcina thermophila, the predominant methanogen prior to H
addition, simultaneously performed acetoclastic, hydrogenotrophic, and methylotrophic methanogenesis. The methanogenic pattern changed after the addition of H
, which immediately stimulated Methanomicrobia-activity and was followed by a slow enrichment of Methanobacteria members. Interestingly, the essential genes involved in the Wood-Ljungdahl pathway were not expressed in bacterial members. The high expression of a glycine cleavage system indicated the activation of alternative metabolic pathways for acetate metabolism, which were reconstructed in the most abundant bacterial genomes. Moreover, as evidenced by predicted auxotrophies, we propose that specific microbes of the community were forming symbiotic relationships, thus reducing the biosynthetic burden of individual members. These results provide new information that will facilitate future microbial ecology studies of interspecies competition and symbiosis in methanogenic niches. Video abstract. |
doi_str_mv | 10.1186/s40168-019-0780-9 |
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. Methanosarcina thermophila, the predominant methanogen prior to H
addition, simultaneously performed acetoclastic, hydrogenotrophic, and methylotrophic methanogenesis. The methanogenic pattern changed after the addition of H
, which immediately stimulated Methanomicrobia-activity and was followed by a slow enrichment of Methanobacteria members. Interestingly, the essential genes involved in the Wood-Ljungdahl pathway were not expressed in bacterial members. The high expression of a glycine cleavage system indicated the activation of alternative metabolic pathways for acetate metabolism, which were reconstructed in the most abundant bacterial genomes. Moreover, as evidenced by predicted auxotrophies, we propose that specific microbes of the community were forming symbiotic relationships, thus reducing the biosynthetic burden of individual members. These results provide new information that will facilitate future microbial ecology studies of interspecies competition and symbiosis in methanogenic niches. Video abstract.</description><identifier>ISSN: 2049-2618</identifier><identifier>EISSN: 2049-2618</identifier><identifier>DOI: 10.1186/s40168-019-0780-9</identifier><identifier>PMID: 32061251</identifier><language>eng</language><publisher>England: BioMed Central</publisher><subject>Acetates - metabolism ; Acetic acid ; Anaerobic digestion ; Anaerobic microorganisms ; Anaerobiosis ; Auxotrophies ; Bacteria - classification ; Bacteria - metabolism ; BASIC BIOLOGICAL SCIENCES ; Biogas ; Bioreactors ; Carbon ; Chemoautotrophic Growth ; Deoxyribonucleic acid ; DNA ; Ecosystem ; Ecosystems ; Gene expression ; Gene Expression Profiling ; Genomes ; Genomics ; Global warming ; Glycine ; glycine cleavage ; Hydrogen - metabolism ; Metabolic Networks and Pathways ; Metabolic pathways ; Metabolic rate ; Metabolism ; Metagenomics ; Metatranscriptomics ; Methane - biosynthesis ; Methanogenesis ; methanogenic pathways ; Methanosarcina - metabolism ; Microbial community ; Microbiology ; Microbiota ; Niches ; Reactors ; Structure-function relationships ; Symbiosis ; Syntrophic acetate oxidation</subject><ispartof>Microbiome, 2020-02, Vol.8 (1), p.22-14, Article 22</ispartof><rights>2020. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s). 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c586t-8ff026f4eabbbf21798a9c5db4052fca1357bf03efec3d50adf934f75e80c6f73</citedby><cites>FETCH-LOGICAL-c586t-8ff026f4eabbbf21798a9c5db4052fca1357bf03efec3d50adf934f75e80c6f73</cites><orcidid>0000-0003-4416-2135 ; 0000000344162135</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7024554/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2357209578?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,44590,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32061251$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1904071$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhu, Xinyu</creatorcontrib><creatorcontrib>Campanaro, Stefano</creatorcontrib><creatorcontrib>Treu, Laura</creatorcontrib><creatorcontrib>Seshadri, Rekha</creatorcontrib><creatorcontrib>Ivanova, Natalia</creatorcontrib><creatorcontrib>Kougias, Panagiotis G</creatorcontrib><creatorcontrib>Kyrpides, Nikos</creatorcontrib><creatorcontrib>Angelidaki, Irini</creatorcontrib><creatorcontrib>USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)</creatorcontrib><title>Metabolic dependencies govern microbial syntrophies during methanogenesis in an anaerobic digestion ecosystem</title><title>Microbiome</title><addtitle>Microbiome</addtitle><description>Methanogenesis, a biological process mediated by complex microbial communities, has attracted great attention due to its contribution to global warming and potential in biotechnological applications. The current study unveiled the core microbial methanogenic metabolisms in anaerobic vessel ecosystems by applying combined genome-centric metagenomics and metatranscriptomics. Here, we demonstrate that an enriched natural system, fueled only with acetate, could support a bacteria-dominated microbiota employing a multi-trophic methanogenic process. Moreover, significant changes, in terms of microbial structure and function, were recorded after the system was supplemented with additional H
. Methanosarcina thermophila, the predominant methanogen prior to H
addition, simultaneously performed acetoclastic, hydrogenotrophic, and methylotrophic methanogenesis. The methanogenic pattern changed after the addition of H
, which immediately stimulated Methanomicrobia-activity and was followed by a slow enrichment of Methanobacteria members. Interestingly, the essential genes involved in the Wood-Ljungdahl pathway were not expressed in bacterial members. The high expression of a glycine cleavage system indicated the activation of alternative metabolic pathways for acetate metabolism, which were reconstructed in the most abundant bacterial genomes. Moreover, as evidenced by predicted auxotrophies, we propose that specific microbes of the community were forming symbiotic relationships, thus reducing the biosynthetic burden of individual members. These results provide new information that will facilitate future microbial ecology studies of interspecies competition and symbiosis in methanogenic niches. Video abstract.</description><subject>Acetates - metabolism</subject><subject>Acetic acid</subject><subject>Anaerobic digestion</subject><subject>Anaerobic microorganisms</subject><subject>Anaerobiosis</subject><subject>Auxotrophies</subject><subject>Bacteria - classification</subject><subject>Bacteria - metabolism</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biogas</subject><subject>Bioreactors</subject><subject>Carbon</subject><subject>Chemoautotrophic Growth</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Ecosystem</subject><subject>Ecosystems</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Global warming</subject><subject>Glycine</subject><subject>glycine cleavage</subject><subject>Hydrogen - metabolism</subject><subject>Metabolic Networks and Pathways</subject><subject>Metabolic pathways</subject><subject>Metabolic rate</subject><subject>Metabolism</subject><subject>Metagenomics</subject><subject>Metatranscriptomics</subject><subject>Methane - biosynthesis</subject><subject>Methanogenesis</subject><subject>methanogenic pathways</subject><subject>Methanosarcina - metabolism</subject><subject>Microbial community</subject><subject>Microbiology</subject><subject>Microbiota</subject><subject>Niches</subject><subject>Reactors</subject><subject>Structure-function relationships</subject><subject>Symbiosis</subject><subject>Syntrophic acetate oxidation</subject><issn>2049-2618</issn><issn>2049-2618</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpVkk2PFCEQhjtG427W_QFeTEfPrQUNDVxMzMaPTdZ40TOhoehhMg0j9JjMv5e2180uIYFQVQ_Fy9s0rwm8J0QOHwoDMsgOiOpASOjUs-aSAlMdHYh8_mh_0VyXsoc6FGGCyZfNRU9hIJSTy2b-josZ0yHY1uERo8NoA5Z2Sn8wx3YONqcxmENbznHJ6bhbg-6UQ5zaGZediWnCiCWUNsTWrNPgWlJ5YcKyhBRbtKmcy4Lzq-aFN4eC1_frVfPry-efN9-6ux9fb28-3XWWy2HppPdAB8_QjOPoKRFKGmW5Gxlw6q0hPRejhx492t5xMM6rnnnBUYIdvOivmtuN65LZ62MOs8lnnUzQ_w5SnrTJS7AH1FIQzg3lHrBnVg7SDwRlL7hD5VCYyvq4sY6ncUZnsepgDk-gTyMx7HSVTwugjHNWAW83QKpq6GLDgnZnU4xoF00UMBCkJr27vyWn36eqm96nU45VJE3raykoLmTNIltW_ZVSMvqHNgjo1RV6c4WurtCrK7SqNW8e9_9Q8d8D_V908LXu</recordid><startdate>20200215</startdate><enddate>20200215</enddate><creator>Zhu, Xinyu</creator><creator>Campanaro, Stefano</creator><creator>Treu, Laura</creator><creator>Seshadri, Rekha</creator><creator>Ivanova, Natalia</creator><creator>Kougias, Panagiotis G</creator><creator>Kyrpides, Nikos</creator><creator>Angelidaki, Irini</creator><general>BioMed Central</general><general>BMC</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-4416-2135</orcidid><orcidid>https://orcid.org/0000000344162135</orcidid></search><sort><creationdate>20200215</creationdate><title>Metabolic dependencies govern microbial syntrophies during methanogenesis in an anaerobic digestion ecosystem</title><author>Zhu, Xinyu ; Campanaro, Stefano ; Treu, Laura ; Seshadri, Rekha ; Ivanova, Natalia ; Kougias, Panagiotis G ; Kyrpides, Nikos ; Angelidaki, Irini</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c586t-8ff026f4eabbbf21798a9c5db4052fca1357bf03efec3d50adf934f75e80c6f73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Acetates - metabolism</topic><topic>Acetic acid</topic><topic>Anaerobic digestion</topic><topic>Anaerobic microorganisms</topic><topic>Anaerobiosis</topic><topic>Auxotrophies</topic><topic>Bacteria - classification</topic><topic>Bacteria - metabolism</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biogas</topic><topic>Bioreactors</topic><topic>Carbon</topic><topic>Chemoautotrophic Growth</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Ecosystem</topic><topic>Ecosystems</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Global warming</topic><topic>Glycine</topic><topic>glycine cleavage</topic><topic>Hydrogen - metabolism</topic><topic>Metabolic Networks and Pathways</topic><topic>Metabolic pathways</topic><topic>Metabolic rate</topic><topic>Metabolism</topic><topic>Metagenomics</topic><topic>Metatranscriptomics</topic><topic>Methane - biosynthesis</topic><topic>Methanogenesis</topic><topic>methanogenic pathways</topic><topic>Methanosarcina - metabolism</topic><topic>Microbial community</topic><topic>Microbiology</topic><topic>Microbiota</topic><topic>Niches</topic><topic>Reactors</topic><topic>Structure-function relationships</topic><topic>Symbiosis</topic><topic>Syntrophic acetate oxidation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhu, Xinyu</creatorcontrib><creatorcontrib>Campanaro, Stefano</creatorcontrib><creatorcontrib>Treu, Laura</creatorcontrib><creatorcontrib>Seshadri, Rekha</creatorcontrib><creatorcontrib>Ivanova, Natalia</creatorcontrib><creatorcontrib>Kougias, Panagiotis G</creatorcontrib><creatorcontrib>Kyrpides, Nikos</creatorcontrib><creatorcontrib>Angelidaki, Irini</creatorcontrib><creatorcontrib>USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)</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 Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</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>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Microbiome</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhu, Xinyu</au><au>Campanaro, Stefano</au><au>Treu, Laura</au><au>Seshadri, Rekha</au><au>Ivanova, Natalia</au><au>Kougias, Panagiotis G</au><au>Kyrpides, Nikos</au><au>Angelidaki, Irini</au><aucorp>USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metabolic dependencies govern microbial syntrophies during methanogenesis in an anaerobic digestion ecosystem</atitle><jtitle>Microbiome</jtitle><addtitle>Microbiome</addtitle><date>2020-02-15</date><risdate>2020</risdate><volume>8</volume><issue>1</issue><spage>22</spage><epage>14</epage><pages>22-14</pages><artnum>22</artnum><issn>2049-2618</issn><eissn>2049-2618</eissn><abstract>Methanogenesis, a biological process mediated by complex microbial communities, has attracted great attention due to its contribution to global warming and potential in biotechnological applications. The current study unveiled the core microbial methanogenic metabolisms in anaerobic vessel ecosystems by applying combined genome-centric metagenomics and metatranscriptomics. Here, we demonstrate that an enriched natural system, fueled only with acetate, could support a bacteria-dominated microbiota employing a multi-trophic methanogenic process. Moreover, significant changes, in terms of microbial structure and function, were recorded after the system was supplemented with additional H
. Methanosarcina thermophila, the predominant methanogen prior to H
addition, simultaneously performed acetoclastic, hydrogenotrophic, and methylotrophic methanogenesis. The methanogenic pattern changed after the addition of H
, which immediately stimulated Methanomicrobia-activity and was followed by a slow enrichment of Methanobacteria members. Interestingly, the essential genes involved in the Wood-Ljungdahl pathway were not expressed in bacterial members. The high expression of a glycine cleavage system indicated the activation of alternative metabolic pathways for acetate metabolism, which were reconstructed in the most abundant bacterial genomes. Moreover, as evidenced by predicted auxotrophies, we propose that specific microbes of the community were forming symbiotic relationships, thus reducing the biosynthetic burden of individual members. These results provide new information that will facilitate future microbial ecology studies of interspecies competition and symbiosis in methanogenic niches. Video abstract.</abstract><cop>England</cop><pub>BioMed Central</pub><pmid>32061251</pmid><doi>10.1186/s40168-019-0780-9</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-4416-2135</orcidid><orcidid>https://orcid.org/0000000344162135</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acetates - metabolism Acetic acid Anaerobic digestion Anaerobic microorganisms Anaerobiosis Auxotrophies Bacteria - classification Bacteria - metabolism BASIC BIOLOGICAL SCIENCES Biogas Bioreactors Carbon Chemoautotrophic Growth Deoxyribonucleic acid DNA Ecosystem Ecosystems Gene expression Gene Expression Profiling Genomes Genomics Global warming Glycine glycine cleavage Hydrogen - metabolism Metabolic Networks and Pathways Metabolic pathways Metabolic rate Metabolism Metagenomics Metatranscriptomics Methane - biosynthesis Methanogenesis methanogenic pathways Methanosarcina - metabolism Microbial community Microbiology Microbiota Niches Reactors Structure-function relationships Symbiosis Syntrophic acetate oxidation |
title | Metabolic dependencies govern microbial syntrophies during methanogenesis in an anaerobic digestion ecosystem |
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