Viruses direct carbon cycling in lake sediments under global change
Global change is altering the vast amount of carbon cycled by microbes between land and freshwater, but how viruses mediate this process is poorly understood. Here, we show that viruses direct carbon cycling in lake sediments, and these impacts intensify with future changes in water clarity and terr...
Gespeichert in:
Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2022-10, Vol.119 (41), p.1-12 |
---|---|
Hauptverfasser: | , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 12 |
---|---|
container_issue | 41 |
container_start_page | 1 |
container_title | Proceedings of the National Academy of Sciences - PNAS |
container_volume | 119 |
creator | Braga, Lucas P. P. Orland, Chloé Emilson, Erik J. S. Fitch, Amelia A. Osterholz, Helena Dittmar, Thorsten Basiliko, Nathan Mykytczuk, Nadia C. S. Tanentzap, Andrew J. |
description | Global change is altering the vast amount of carbon cycled by microbes between land and freshwater, but how viruses mediate this process is poorly understood. Here, we show that viruses direct carbon cycling in lake sediments, and these impacts intensify with future changes in water clarity and terrestrial organic matter (tOM) inputs. Using experimental tOM gradients within sediments of a clear and a dark boreal lake, we identified 156 viral operational taxonomic units (vOTUs), of which 21% strongly increased with abundances of key bacteria and archaea, identified via metagenomeassembled genomes (MAGs). MAGs included the most abundant prokaryotes, which were themselves associated with dissolved organic matter (DOM) composition and greenhouse gas (GHG) concentrations. Increased abundances of virus-like particles were separately associated with reduced bacterial metabolism and with shifts in DOM toward amino sugars, likely released by cell lysis rather than higher molecular mass compounds accumulating from reduced tOM degradation. An additional 9.6% of vOTUs harbored auxiliary metabolic genes associated with DOM and GHGs. Taken together, these different effects on host dynamics and metabolism can explain why abundances of vOTUs rather than MAGs were better overall predictors of carbon cycling. Future increases in tOM quantity, but not quality, will change viral composition and function with consequences for DOM pools. Given their importance, viruses must now be explicitly considered in efforts to understand and predict the freshwater carbon cycle and its future under global environmental change. |
doi_str_mv | 10.1073/pnas.2202261119 |
format | Article |
fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9564219</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>27208793</jstor_id><sourcerecordid>27208793</sourcerecordid><originalsourceid>FETCH-LOGICAL-c443t-7fa767db663843df9a1714442a1d3de460ab9f8a6d5e516b4b1586ae5c12f7af3</originalsourceid><addsrcrecordid>eNpdkb1vFDEQxS1ERI5ATUVkiYZmE3973SBFJyCRIqVJaK1Z23vxsWdf7N1I-e_Z04ULpJri_ebNPD2EPlFyRonm59sE9YwxwpiilJo3aEGJoY0ShrxFC0KYblrBxDF6X-uaEGJkS96hY64YUVyZBVr-imWqoWIfS3AjdlC6nLB7ckNMKxwTHuB3wDX4uAlprHhKPhS8GnIHA3b3kFbhAzrqYajh4_M8QXc_vt8uL5vrm59Xy4vrxgnBx0b3oJX2nVK8Fdz3BqimQggG1HMfhCLQmb4F5WWQVHWio7JVEKSjrNfQ8xP0be-7nbpN8G7-p8BgtyVuoDzZDNH-r6R4b1f50RqpBKNmNvj6bFDywxTqaDexujAMkEKeqmWacSpla_SMfnmFrvNU0hxvRykitZJyps73lCu51hL6wzOU2F1BdleQfSlo3jj9N8OB_9vIDHzeA-s65nLQ56Ok1YbzPywvlj0</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2726057655</pqid></control><display><type>article</type><title>Viruses direct carbon cycling in lake sediments under global change</title><source>MEDLINE</source><source>Full-Text Journals in Chemistry (Open access)</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><creator>Braga, Lucas P. P. ; Orland, Chloé ; Emilson, Erik J. S. ; Fitch, Amelia A. ; Osterholz, Helena ; Dittmar, Thorsten ; Basiliko, Nathan ; Mykytczuk, Nadia C. S. ; Tanentzap, Andrew J.</creator><creatorcontrib>Braga, Lucas P. P. ; Orland, Chloé ; Emilson, Erik J. S. ; Fitch, Amelia A. ; Osterholz, Helena ; Dittmar, Thorsten ; Basiliko, Nathan ; Mykytczuk, Nadia C. S. ; Tanentzap, Andrew J.</creatorcontrib><description>Global change is altering the vast amount of carbon cycled by microbes between land and freshwater, but how viruses mediate this process is poorly understood. Here, we show that viruses direct carbon cycling in lake sediments, and these impacts intensify with future changes in water clarity and terrestrial organic matter (tOM) inputs. Using experimental tOM gradients within sediments of a clear and a dark boreal lake, we identified 156 viral operational taxonomic units (vOTUs), of which 21% strongly increased with abundances of key bacteria and archaea, identified via metagenomeassembled genomes (MAGs). MAGs included the most abundant prokaryotes, which were themselves associated with dissolved organic matter (DOM) composition and greenhouse gas (GHG) concentrations. Increased abundances of virus-like particles were separately associated with reduced bacterial metabolism and with shifts in DOM toward amino sugars, likely released by cell lysis rather than higher molecular mass compounds accumulating from reduced tOM degradation. An additional 9.6% of vOTUs harbored auxiliary metabolic genes associated with DOM and GHGs. Taken together, these different effects on host dynamics and metabolism can explain why abundances of vOTUs rather than MAGs were better overall predictors of carbon cycling. Future increases in tOM quantity, but not quality, will change viral composition and function with consequences for DOM pools. Given their importance, viruses must now be explicitly considered in efforts to understand and predict the freshwater carbon cycle and its future under global environmental change.</description><identifier>ISSN: 0027-8424</identifier><identifier>ISSN: 1091-6490</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2202261119</identifier><identifier>PMID: 36206369</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Abundance ; Amino Sugars - metabolism ; Archaea ; Bacteria - genetics ; Bacteria - metabolism ; Biological Sciences ; Carbon ; Carbon - metabolism ; Carbon Cycle ; Dissolved organic matter ; Environmental changes ; Genomes ; Greenhouse effect ; Greenhouse gases ; Greenhouse Gases - metabolism ; Lake sediments ; Lakes ; Lakes - microbiology ; Lysis ; Metabolism ; Prokaryotes ; Sediments ; Sugar ; Virus-like particles ; Viruses ; Viruses - genetics ; Viruses - metabolism ; Water - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2022-10, Vol.119 (41), p.1-12</ispartof><rights>Copyright © 2022 the Author(s)</rights><rights>Copyright National Academy of Sciences Oct 11, 2022</rights><rights>Copyright © 2022 the Author(s). Published by PNAS. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-7fa767db663843df9a1714442a1d3de460ab9f8a6d5e516b4b1586ae5c12f7af3</citedby><cites>FETCH-LOGICAL-c443t-7fa767db663843df9a1714442a1d3de460ab9f8a6d5e516b4b1586ae5c12f7af3</cites><orcidid>0000-0003-2789-7252 ; 0000-0002-2883-1901 ; 0000-0003-1757-2219 ; 0000-0002-2858-9799 ; 0000-0002-1516-9728</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/PMC9564219/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9564219/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36206369$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Braga, Lucas P. P.</creatorcontrib><creatorcontrib>Orland, Chloé</creatorcontrib><creatorcontrib>Emilson, Erik J. S.</creatorcontrib><creatorcontrib>Fitch, Amelia A.</creatorcontrib><creatorcontrib>Osterholz, Helena</creatorcontrib><creatorcontrib>Dittmar, Thorsten</creatorcontrib><creatorcontrib>Basiliko, Nathan</creatorcontrib><creatorcontrib>Mykytczuk, Nadia C. S.</creatorcontrib><creatorcontrib>Tanentzap, Andrew J.</creatorcontrib><title>Viruses direct carbon cycling in lake sediments under global change</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Global change is altering the vast amount of carbon cycled by microbes between land and freshwater, but how viruses mediate this process is poorly understood. Here, we show that viruses direct carbon cycling in lake sediments, and these impacts intensify with future changes in water clarity and terrestrial organic matter (tOM) inputs. Using experimental tOM gradients within sediments of a clear and a dark boreal lake, we identified 156 viral operational taxonomic units (vOTUs), of which 21% strongly increased with abundances of key bacteria and archaea, identified via metagenomeassembled genomes (MAGs). MAGs included the most abundant prokaryotes, which were themselves associated with dissolved organic matter (DOM) composition and greenhouse gas (GHG) concentrations. Increased abundances of virus-like particles were separately associated with reduced bacterial metabolism and with shifts in DOM toward amino sugars, likely released by cell lysis rather than higher molecular mass compounds accumulating from reduced tOM degradation. An additional 9.6% of vOTUs harbored auxiliary metabolic genes associated with DOM and GHGs. Taken together, these different effects on host dynamics and metabolism can explain why abundances of vOTUs rather than MAGs were better overall predictors of carbon cycling. Future increases in tOM quantity, but not quality, will change viral composition and function with consequences for DOM pools. Given their importance, viruses must now be explicitly considered in efforts to understand and predict the freshwater carbon cycle and its future under global environmental change.</description><subject>Abundance</subject><subject>Amino Sugars - metabolism</subject><subject>Archaea</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Biological Sciences</subject><subject>Carbon</subject><subject>Carbon - metabolism</subject><subject>Carbon Cycle</subject><subject>Dissolved organic matter</subject><subject>Environmental changes</subject><subject>Genomes</subject><subject>Greenhouse effect</subject><subject>Greenhouse gases</subject><subject>Greenhouse Gases - metabolism</subject><subject>Lake sediments</subject><subject>Lakes</subject><subject>Lakes - microbiology</subject><subject>Lysis</subject><subject>Metabolism</subject><subject>Prokaryotes</subject><subject>Sediments</subject><subject>Sugar</subject><subject>Virus-like particles</subject><subject>Viruses</subject><subject>Viruses - genetics</subject><subject>Viruses - metabolism</subject><subject>Water - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkb1vFDEQxS1ERI5ATUVkiYZmE3973SBFJyCRIqVJaK1Z23vxsWdf7N1I-e_Z04ULpJri_ebNPD2EPlFyRonm59sE9YwxwpiilJo3aEGJoY0ShrxFC0KYblrBxDF6X-uaEGJkS96hY64YUVyZBVr-imWqoWIfS3AjdlC6nLB7ckNMKxwTHuB3wDX4uAlprHhKPhS8GnIHA3b3kFbhAzrqYajh4_M8QXc_vt8uL5vrm59Xy4vrxgnBx0b3oJX2nVK8Fdz3BqimQggG1HMfhCLQmb4F5WWQVHWio7JVEKSjrNfQ8xP0be-7nbpN8G7-p8BgtyVuoDzZDNH-r6R4b1f50RqpBKNmNvj6bFDywxTqaDexujAMkEKeqmWacSpla_SMfnmFrvNU0hxvRykitZJyps73lCu51hL6wzOU2F1BdleQfSlo3jj9N8OB_9vIDHzeA-s65nLQ56Ok1YbzPywvlj0</recordid><startdate>20221011</startdate><enddate>20221011</enddate><creator>Braga, Lucas P. P.</creator><creator>Orland, Chloé</creator><creator>Emilson, Erik J. S.</creator><creator>Fitch, Amelia A.</creator><creator>Osterholz, Helena</creator><creator>Dittmar, Thorsten</creator><creator>Basiliko, Nathan</creator><creator>Mykytczuk, Nadia C. S.</creator><creator>Tanentzap, Andrew J.</creator><general>National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2789-7252</orcidid><orcidid>https://orcid.org/0000-0002-2883-1901</orcidid><orcidid>https://orcid.org/0000-0003-1757-2219</orcidid><orcidid>https://orcid.org/0000-0002-2858-9799</orcidid><orcidid>https://orcid.org/0000-0002-1516-9728</orcidid></search><sort><creationdate>20221011</creationdate><title>Viruses direct carbon cycling in lake sediments under global change</title><author>Braga, Lucas P. P. ; Orland, Chloé ; Emilson, Erik J. S. ; Fitch, Amelia A. ; Osterholz, Helena ; Dittmar, Thorsten ; Basiliko, Nathan ; Mykytczuk, Nadia C. S. ; Tanentzap, Andrew J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c443t-7fa767db663843df9a1714442a1d3de460ab9f8a6d5e516b4b1586ae5c12f7af3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Abundance</topic><topic>Amino Sugars - metabolism</topic><topic>Archaea</topic><topic>Bacteria - genetics</topic><topic>Bacteria - metabolism</topic><topic>Biological Sciences</topic><topic>Carbon</topic><topic>Carbon - metabolism</topic><topic>Carbon Cycle</topic><topic>Dissolved organic matter</topic><topic>Environmental changes</topic><topic>Genomes</topic><topic>Greenhouse effect</topic><topic>Greenhouse gases</topic><topic>Greenhouse Gases - metabolism</topic><topic>Lake sediments</topic><topic>Lakes</topic><topic>Lakes - microbiology</topic><topic>Lysis</topic><topic>Metabolism</topic><topic>Prokaryotes</topic><topic>Sediments</topic><topic>Sugar</topic><topic>Virus-like particles</topic><topic>Viruses</topic><topic>Viruses - genetics</topic><topic>Viruses - metabolism</topic><topic>Water - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Braga, Lucas P. P.</creatorcontrib><creatorcontrib>Orland, Chloé</creatorcontrib><creatorcontrib>Emilson, Erik J. S.</creatorcontrib><creatorcontrib>Fitch, Amelia A.</creatorcontrib><creatorcontrib>Osterholz, Helena</creatorcontrib><creatorcontrib>Dittmar, Thorsten</creatorcontrib><creatorcontrib>Basiliko, Nathan</creatorcontrib><creatorcontrib>Mykytczuk, Nadia C. S.</creatorcontrib><creatorcontrib>Tanentzap, Andrew J.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Braga, Lucas P. P.</au><au>Orland, Chloé</au><au>Emilson, Erik J. S.</au><au>Fitch, Amelia A.</au><au>Osterholz, Helena</au><au>Dittmar, Thorsten</au><au>Basiliko, Nathan</au><au>Mykytczuk, Nadia C. S.</au><au>Tanentzap, Andrew J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Viruses direct carbon cycling in lake sediments under global change</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2022-10-11</date><risdate>2022</risdate><volume>119</volume><issue>41</issue><spage>1</spage><epage>12</epage><pages>1-12</pages><issn>0027-8424</issn><issn>1091-6490</issn><eissn>1091-6490</eissn><abstract>Global change is altering the vast amount of carbon cycled by microbes between land and freshwater, but how viruses mediate this process is poorly understood. Here, we show that viruses direct carbon cycling in lake sediments, and these impacts intensify with future changes in water clarity and terrestrial organic matter (tOM) inputs. Using experimental tOM gradients within sediments of a clear and a dark boreal lake, we identified 156 viral operational taxonomic units (vOTUs), of which 21% strongly increased with abundances of key bacteria and archaea, identified via metagenomeassembled genomes (MAGs). MAGs included the most abundant prokaryotes, which were themselves associated with dissolved organic matter (DOM) composition and greenhouse gas (GHG) concentrations. Increased abundances of virus-like particles were separately associated with reduced bacterial metabolism and with shifts in DOM toward amino sugars, likely released by cell lysis rather than higher molecular mass compounds accumulating from reduced tOM degradation. An additional 9.6% of vOTUs harbored auxiliary metabolic genes associated with DOM and GHGs. Taken together, these different effects on host dynamics and metabolism can explain why abundances of vOTUs rather than MAGs were better overall predictors of carbon cycling. Future increases in tOM quantity, but not quality, will change viral composition and function with consequences for DOM pools. Given their importance, viruses must now be explicitly considered in efforts to understand and predict the freshwater carbon cycle and its future under global environmental change.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>36206369</pmid><doi>10.1073/pnas.2202261119</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-2789-7252</orcidid><orcidid>https://orcid.org/0000-0002-2883-1901</orcidid><orcidid>https://orcid.org/0000-0003-1757-2219</orcidid><orcidid>https://orcid.org/0000-0002-2858-9799</orcidid><orcidid>https://orcid.org/0000-0002-1516-9728</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0027-8424 |
ispartof | Proceedings of the National Academy of Sciences - PNAS, 2022-10, Vol.119 (41), p.1-12 |
issn | 0027-8424 1091-6490 1091-6490 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9564219 |
source | MEDLINE; Full-Text Journals in Chemistry (Open access); PubMed Central; Alma/SFX Local Collection |
subjects | Abundance Amino Sugars - metabolism Archaea Bacteria - genetics Bacteria - metabolism Biological Sciences Carbon Carbon - metabolism Carbon Cycle Dissolved organic matter Environmental changes Genomes Greenhouse effect Greenhouse gases Greenhouse Gases - metabolism Lake sediments Lakes Lakes - microbiology Lysis Metabolism Prokaryotes Sediments Sugar Virus-like particles Viruses Viruses - genetics Viruses - metabolism Water - metabolism |
title | Viruses direct carbon cycling in lake sediments under global change |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-10T16%3A20%3A53IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Viruses%20direct%20carbon%20cycling%20in%20lake%20sediments%20under%20global%20change&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Braga,%20Lucas%20P.%20P.&rft.date=2022-10-11&rft.volume=119&rft.issue=41&rft.spage=1&rft.epage=12&rft.pages=1-12&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.2202261119&rft_dat=%3Cjstor_pubme%3E27208793%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2726057655&rft_id=info:pmid/36206369&rft_jstor_id=27208793&rfr_iscdi=true |