Decoupling of respiration rates and abundance in marine prokaryoplankton

The ocean-atmosphere exchange of CO2 largely depends on the balance between marine microbial photosynthesis and respiration. Despite vast taxonomic and metabolic diversity among marine planktonic bacteria and archaea (prokaryoplankton)1-3, their respiration usually is measured in bulk and treated as...

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Detalles Bibliográficos
Autores: Munson-McGee, Jacob H, Lindsay, Melody R, Sintes, Eva, Brown, Julia M, D'Angelo, Timothy, Brown, Joe, Lubelczyk, Laura C, Tomko, Paxton, Emerson, David, Orcutt, Beth N., Poulton, Nicole J, Herndl, Gerhard J, Stepanauskas, Ramunas
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/341322
Acceso en línea:http://hdl.handle.net/10261/341322
https://api.elsevier.com/content/abstract/scopus_id/85143504356
Access Level:acceso abierto
Palabra clave:Bacterial physiology
Marine microbiology
Metagenomics
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spelling Decoupling of respiration rates and abundance in marine prokaryoplanktonMunson-McGee, Jacob HLindsay, Melody RSintes, EvaBrown, Julia MD'Angelo, TimothyBrown, JoeLubelczyk, Laura CTomko, PaxtonEmerson, DavidOrcutt, Beth N.Poulton, Nicole JHerndl, Gerhard JStepanauskas, RamunasBacterial physiologyMarine microbiologyMetagenomicsThe ocean-atmosphere exchange of CO2 largely depends on the balance between marine microbial photosynthesis and respiration. Despite vast taxonomic and metabolic diversity among marine planktonic bacteria and archaea (prokaryoplankton)1-3, their respiration usually is measured in bulk and treated as a 'black box' in global biogeochemical models4; this limits the mechanistic understanding of the global carbon cycle. Here, using a technology for integrated phenotype analyses and genomic sequencing of individual microbial cells, we show that cell-specific respiration rates differ by more than 1,000× among prokaryoplankton genera. The majority of respiration was found to be performed by minority members of prokaryoplankton (including the Roseobacter cluster), whereas cells of the most prevalent lineages (including Pelagibacter and SAR86) had extremely low respiration rates. The decoupling of respiration rates from abundance among lineages, elevated counts of proteorhodopsin transcripts in Pelagibacter and SAR86 cells and elevated respiration of SAR86 at night indicate that proteorhodopsin-based phototrophy3,5-7 probably constitutes an important source of energy to prokaryoplankton and may increase growth efficiency. These findings suggest that the dependence of prokaryoplankton on respiration and remineralization of phytoplankton-derived organic carbon into CO2 for its energy demands and growth may be lower than commonly assumed and variable among lineages.This work was supported by awards from the US National Science Foundation (1826734 to R.S., D.E., B.N.O. and N.J.P.; 1737017 to B.N.O.; and 1335810 to R.S.), the Austrian Science Fund (FWF) project ARTEMIS (P28781-B21 to G.J.H.) and by the Simons Foundation grant (827839 to R.S.).Peer reviewedNature Publishing GroupNational Science Foundation (US)Simons FoundationConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232022info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/341322https://api.elsevier.com/content/abstract/scopus_id/85143504356reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésNaturehttps://doi.org/10.1038/s41586-022-05505-3Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3413222026-05-22T06:33:51Z
dc.title.none.fl_str_mv Decoupling of respiration rates and abundance in marine prokaryoplankton
title Decoupling of respiration rates and abundance in marine prokaryoplankton
spellingShingle Decoupling of respiration rates and abundance in marine prokaryoplankton
Munson-McGee, Jacob H
Bacterial physiology
Marine microbiology
Metagenomics
title_short Decoupling of respiration rates and abundance in marine prokaryoplankton
title_full Decoupling of respiration rates and abundance in marine prokaryoplankton
title_fullStr Decoupling of respiration rates and abundance in marine prokaryoplankton
title_full_unstemmed Decoupling of respiration rates and abundance in marine prokaryoplankton
title_sort Decoupling of respiration rates and abundance in marine prokaryoplankton
dc.creator.none.fl_str_mv Munson-McGee, Jacob H
Lindsay, Melody R
Sintes, Eva
Brown, Julia M
D'Angelo, Timothy
Brown, Joe
Lubelczyk, Laura C
Tomko, Paxton
Emerson, David
Orcutt, Beth N.
Poulton, Nicole J
Herndl, Gerhard J
Stepanauskas, Ramunas
author Munson-McGee, Jacob H
author_facet Munson-McGee, Jacob H
Lindsay, Melody R
Sintes, Eva
Brown, Julia M
D'Angelo, Timothy
Brown, Joe
Lubelczyk, Laura C
Tomko, Paxton
Emerson, David
Orcutt, Beth N.
Poulton, Nicole J
Herndl, Gerhard J
Stepanauskas, Ramunas
author_role author
author2 Lindsay, Melody R
Sintes, Eva
Brown, Julia M
D'Angelo, Timothy
Brown, Joe
Lubelczyk, Laura C
Tomko, Paxton
Emerson, David
Orcutt, Beth N.
Poulton, Nicole J
Herndl, Gerhard J
Stepanauskas, Ramunas
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv National Science Foundation (US)
Simons Foundation
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Bacterial physiology
Marine microbiology
Metagenomics
topic Bacterial physiology
Marine microbiology
Metagenomics
description The ocean-atmosphere exchange of CO2 largely depends on the balance between marine microbial photosynthesis and respiration. Despite vast taxonomic and metabolic diversity among marine planktonic bacteria and archaea (prokaryoplankton)1-3, their respiration usually is measured in bulk and treated as a 'black box' in global biogeochemical models4; this limits the mechanistic understanding of the global carbon cycle. Here, using a technology for integrated phenotype analyses and genomic sequencing of individual microbial cells, we show that cell-specific respiration rates differ by more than 1,000× among prokaryoplankton genera. The majority of respiration was found to be performed by minority members of prokaryoplankton (including the Roseobacter cluster), whereas cells of the most prevalent lineages (including Pelagibacter and SAR86) had extremely low respiration rates. The decoupling of respiration rates from abundance among lineages, elevated counts of proteorhodopsin transcripts in Pelagibacter and SAR86 cells and elevated respiration of SAR86 at night indicate that proteorhodopsin-based phototrophy3,5-7 probably constitutes an important source of energy to prokaryoplankton and may increase growth efficiency. These findings suggest that the dependence of prokaryoplankton on respiration and remineralization of phytoplankton-derived organic carbon into CO2 for its energy demands and growth may be lower than commonly assumed and variable among lineages.
publishDate 2022
dc.date.none.fl_str_mv 2022
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/341322
https://api.elsevier.com/content/abstract/scopus_id/85143504356
url http://hdl.handle.net/10261/341322
https://api.elsevier.com/content/abstract/scopus_id/85143504356
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Nature
https://doi.org/10.1038/s41586-022-05505-3
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Nature Publishing Group
publisher.none.fl_str_mv Nature Publishing Group
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.812429

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