Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans

Background Prokaryotic microbes have impacted marine biogeochemical cycles for billions of years. Viruses also impact these cycles, through lysis, horizontal gene transfer, and encoding and expressing genes that contribute to metabolic reprogramming of prokaryotic cells. While this impact is difficu...

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Autores: Tian, Funing, Wainaina, James M., Howard-Varona, Cristina, Domínguez-Huerta, Guillermo, Bolduc, Benjamin, Gazitúa, María Consuelo, Smith, Garrett, Gittrich, Marissa R., Zablocki, Olivier, Cronin, Dylan R., Eveillard, Damien, Hallam, Steven J., Sullivan, Matthew B.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/386528
Acceso en línea:http://hdl.handle.net/10261/386528
https://api.elsevier.com/content/abstract/scopus_id/85202909517
Access Level:acceso abierto
Palabra clave:Tara Oceans
AMGs
Prokaryotic
id ES_e01e2d18b2fdefc2d0b316506c845df0
oai_identifier_str oai:digital.csic.es:10261/386528
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
title Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
spellingShingle Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
Tian, Funing
Tara Oceans
AMGs
Prokaryotic
title_short Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
title_full Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
title_fullStr Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
title_full_unstemmed Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
title_sort Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
dc.creator.none.fl_str_mv Tian, Funing
Wainaina, James M.
Howard-Varona, Cristina
Domínguez-Huerta, Guillermo
Bolduc, Benjamin
Gazitúa, María Consuelo
Smith, Garrett
Gittrich, Marissa R.
Zablocki, Olivier
Cronin, Dylan R.
Eveillard, Damien
Hallam, Steven J.
Sullivan, Matthew B.
author Tian, Funing
author_facet Tian, Funing
Wainaina, James M.
Howard-Varona, Cristina
Domínguez-Huerta, Guillermo
Bolduc, Benjamin
Gazitúa, María Consuelo
Smith, Garrett
Gittrich, Marissa R.
Zablocki, Olivier
Cronin, Dylan R.
Eveillard, Damien
Hallam, Steven J.
Sullivan, Matthew B.
author_role author
author2 Wainaina, James M.
Howard-Varona, Cristina
Domínguez-Huerta, Guillermo
Bolduc, Benjamin
Gazitúa, María Consuelo
Smith, Garrett
Gittrich, Marissa R.
Zablocki, Olivier
Cronin, Dylan R.
Eveillard, Damien
Hallam, Steven J.
Sullivan, Matthew B.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv National Science Foundation (US)
Gordon and Betty Moore Foundation
Natural Sciences and Engineering Research Council of Canada
Canada Foundation for Innovation
Ohio Supercomputer Center
Ambrose Monell Foundation
G. Unger Vetlesen Foundation
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Tara Oceans
AMGs
Prokaryotic
topic Tara Oceans
AMGs
Prokaryotic
description Background Prokaryotic microbes have impacted marine biogeochemical cycles for billions of years. Viruses also impact these cycles, through lysis, horizontal gene transfer, and encoding and expressing genes that contribute to metabolic reprogramming of prokaryotic cells. While this impact is difficult to quantify in nature, we hypothesized that it can be examined by surveying virus-encoded auxiliary metabolic genes (AMGs) and assessing their ecological context.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
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/10261/386528
https://api.elsevier.com/content/abstract/scopus_id/85202909517
url http://hdl.handle.net/10261/386528
https://api.elsevier.com/content/abstract/scopus_id/85202909517
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Centro Oceanográfico de Málaga, (COMA)
Tian, Funing,; Wainaina, James M.; Bolduc, Benjamin ; Sullivan, Matthew B.; 2024; Virus-encoded auxiliary metabolic genes throughout the global oceans [Dataset]. Zenodo; https://doi.org/10.5281/zenodo.12668289
Tian, Funing; Wainaina, James M.; Howard-Varona, Cristina; Domínguez-Huerta, Guillermo; Bolduc, Benjamin; Gazitúa, María Consuelo; Smith, Garrett; Gittrich, Marissa R.; Zablocki, Olivier; Cronin, Dylan R.; Eveillard, Damien ; Hallam, Steven J.; Sullivan, Matthew B.; 2024; Additional file 1 of Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans [Dataset]; Figshare; https://doi.org/10.6084/m9.figshare.26943933.v1
https://doi.org/10.1186/s40168-024-01876-z
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
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
_version_ 1869422172696477696
spelling Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceansTian, FuningWainaina, James M.Howard-Varona, CristinaDomínguez-Huerta, GuillermoBolduc, BenjaminGazitúa, María ConsueloSmith, GarrettGittrich, Marissa R.Zablocki, OlivierCronin, Dylan R.Eveillard, DamienHallam, Steven J.Sullivan, Matthew B.Tara OceansAMGsProkaryoticBackground Prokaryotic microbes have impacted marine biogeochemical cycles for billions of years. Viruses also impact these cycles, through lysis, horizontal gene transfer, and encoding and expressing genes that contribute to metabolic reprogramming of prokaryotic cells. While this impact is difficult to quantify in nature, we hypothesized that it can be examined by surveying virus-encoded auxiliary metabolic genes (AMGs) and assessing their ecological context.Results We systematically developed a global ocean AMG catalog by integrating previously described and newly identified AMGs and then placed this catalog into ecological and metabolic contexts relevant to ocean biogeochemistry. From 7.6 terabases of Tara Oceans paired prokaryote- and virus-enriched metagenomic sequence data, we increased known ocean virus populations to 579,904 (up 16%). From these virus populations, we then conservatively identified 86,913 AMGs that grouped into 22,779 sequence-based gene clusters, 7248 (~ 32%) of which were not previously reported. Using our catalog and modeled data from mock communities, we estimate that ~ 19% of ocean virus populations carry at least one AMG. To understand AMGs in their metabolic context, we identified 340 metabolic pathways encoded by ocean microbes and showed that AMGs map to 128 of them. Furthermore, we identified metabolic “hot spots” targeted by virus AMGs, including nine pathways where most steps (≥ 0.75) were AMG-targeted (involved in carbohydrate, amino acid, fatty acid, and nucleotide metabolism), as well as other pathways where virus-encoded AMGs outnumbered cellular homologs (involved in lipid A phosphates, phosphatidylethanolamine, creatine biosynthesis, phosphoribosylamine-glycine ligase, and carbamoyl-phosphate synthase pathways).Conclusions Together, this systematically curated, global ocean AMG catalog and analyses provide a valuable resource and foundational observations to understand the role of viruses in modulating global ocean metabolisms and their biogeochemical implications.Funding was provided by the National Science Foundation (awards ABI#1759874, ABI#2149505, OCE#1536989, OCE#1829831, and OCE#2019589) and a Gordon and Betty Moore Foundation Investigator Award (#3790) to MBS and by the Natural Sciences and Engineering Research Council (NSERC) of Canada, the Canada Foundation for Innovation (CFI), and the G. Unger Vetlesen and Ambrose Monell Foundations to SJH. Bioinformatics analysis was supported by Ohio Supercomputer Center.Peer reviewedBioMed CentralNational Science Foundation (US)Gordon and Betty Moore FoundationNatural Sciences and Engineering Research Council of CanadaCanada Foundation for InnovationOhio Supercomputer CenterAmbrose Monell FoundationG. Unger Vetlesen FoundationConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/386528https://api.elsevier.com/content/abstract/scopus_id/85202909517reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésCentro Oceanográfico de Málaga, (COMA)Tian, Funing,; Wainaina, James M.; Bolduc, Benjamin ; Sullivan, Matthew B.; 2024; Virus-encoded auxiliary metabolic genes throughout the global oceans [Dataset]. Zenodo; https://doi.org/10.5281/zenodo.12668289Tian, Funing; Wainaina, James M.; Howard-Varona, Cristina; Domínguez-Huerta, Guillermo; Bolduc, Benjamin; Gazitúa, María Consuelo; Smith, Garrett; Gittrich, Marissa R.; Zablocki, Olivier; Cronin, Dylan R.; Eveillard, Damien ; Hallam, Steven J.; Sullivan, Matthew B.; 2024; Additional file 1 of Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans [Dataset]; Figshare; https://doi.org/10.6084/m9.figshare.26943933.v1https://doi.org/10.1186/s40168-024-01876-zSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3865282026-05-22T06:33:51Z
score 15,81155

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