Caudovirales bacteriophages are associated with improved executive function and memory in flies, mice, and humans

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• dc.contributor.author Mayneris Perxachs, Jordi
• dc.contributor.author Castells-Nobau, Anna
• dc.contributor.author Arnoriaga Rodríguez, María
• dc.contributor.author Garre-Olmo, Josep
• dc.contributor.author Puig, Josep
• dc.contributor.author Ramos, Rafel
• dc.contributor.author Martínez Hernández, Francisco
• dc.contributor.author Burokas, Aurelijus, 1982-
• dc.contributor.author Coll, Clàudia
• dc.contributor.author Moreno-Navarrete, José Maria
• dc.contributor.author Zapata-Tona, Cristina
• dc.contributor.author Pedraza, Salvador
• dc.contributor.author Pérez Brocal, Vicente
• dc.contributor.author Ramió-Torrentà, Lluís
• dc.contributor.author Ricart, Wifredo
• dc.contributor.author Moya, Andrés
• dc.contributor.author Martínez García, Manuel
• dc.contributor.author Maldonado, Rafael, 1961-
• dc.contributor.author Fernández Real, Jose M.
• dc.date.accessioned 2022-04-25T06:36:53Z
• dc.date.available 2022-04-25T06:36:53Z
• dc.date.issued 2022
• dc.description.abstract Growing evidence implicates the gut microbiome in cognition. Viruses, the most abundant life entities on the planet, are a commonly overlooked component of the gut virome, dominated by the Caudovirales and Microviridae bacteriophages. Here, we show in a discovery (n = 114) and a validation cohort (n = 942) that subjects with increased Caudovirales and Siphoviridae levels in the gut microbiome had better performance in executive processes and verbal memory. Conversely, increased Microviridae levels were linked to a greater impairment in executive abilities. Microbiota transplantation from human donors with increased specific Caudovirales (>90% from the Siphoviridae family) levels led to increased scores in the novel object recognition test in mice and up-regulated memory-promoting immediate early genes in the prefrontal cortex. Supplementation of the Drosophila diet with the 936 group of lactococcal Siphoviridae bacteriophages resulted in increased memory scores and upregulation of memory-involved brain genes. Thus, bacteriophages warrant consideration as novel actors in the microbiome-brain axis.
• dc.description.sponsorship This work was partially funded by the Instituto de Salud Carlos III (Madrid, Spain) through the project PI15/01934, PI18/01022, PI21/01361) to J.M.F.-R. and the project PI20/01090 (co-funded by the European Regional Development Fund . “A way to make Europe”) to J.M.-P., the grants SAF2015-65878-R from the Ministry of Economy and Competitiveness , Prometeo/2018/A/133 from Generalitat Valenciana, Spain and also by the Fondo Europeo de Desarrollo Regional (FEDER) funds, European Commission (FP7, NeuroPain #2013- 602891 ), the Catalan Government (AGAUR, #SGR2017-669 , #2017 SGR- 734, ICREA Academia Award 2015 to R.M. and ICREA Academia Award 2022 to J.M.F.R.), the Spanish Instituto de Salud Carlos III (RTA, #RD16/0017/0020 ), the European Regional Development Fund (project No. 01.2.2-LMT-K-718-02-0014) under grant agreement with the Research Council of Lithuania (LMTLT), and the Project ThinkGut (EFA345/19) 65% co-financed by the European Regional Development Fund (ERDF) through the Interreg V-A Spain-France-Andorra programme (POCTEFA 2014-2020). CIBERobn is also co-funded by the European Regional Development Fund. We also acknowledge the funding from the Spanish Ministry of Science, Innovation and Universities ( RTI2018-099200-B-I00 ), and the Generalitat of Catalonia (Agency for Management of University and Research grants ( 2017SGR696 ) and Department of Health (SLT002/16/00250)) to R.M M.A.-R. is funded by the Instituto de Salud Carlos III , Río Hortega ( CM19/00190 ). J.M.-P. is funded by the Miguel Servet Program from the Instituto de Salud Carlos III ( ISCIII CP18/00009 ), co-funded by the European Social Fund “Investing in your future.” A.C.-N. is funded by the Instituto de Salud Carlos III , Sara Borrell. MMG was funded by the Spanish Ministry of Science, Innovation and Universities RTI2018-094248-B-I00.
• dc.format.mimetype application/pdf
• dc.identifier.citation Mayneris-Perxachs J, Castells-Nobau A, Arnoriaga-Rodríguez M, Garre-Olmo J, Puig J, Ramos R, Martínez-Hernández F, Burokas A, Coll C, Moreno-Navarrete JM, Zapata-Tona C, Pedraza S, Pérez-Brocal V, Ramió-Torrentà L, Ricart W, Moya A, Martínez-García M, Maldonado R, Fernández-Real JM. Caudovirales bacteriophages are associated with improved executive function and memory in flies, mice, and humans. Cell Host Microbe. 2022 Mar 9;30(3):340-56.e8. DOI: 10.1016/j.chom.2022.01.013
• dc.identifier.doi http://dx.doi.org/10.1016/j.chom.2022.01.013
• dc.identifier.issn 1931-3128
• dc.identifier.uri http://hdl.handle.net/10230/52878
• dc.language.iso eng
• dc.publisher Elsevier
• dc.relation.ispartof Cell Host Microbe. 2022 Mar 9;30(3):340-56.e8
• dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/602891
• dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/SAF2015-65878-R
• dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/RTI2018-099200-B-I00
• dc.rights © 2022 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by-nc-nd/4.0/
• dc.subject.keyword Drosophila
• dc.subject.keyword Bacteriophages
• dc.subject.keyword Brain
• dc.subject.keyword Cognition
• dc.subject.keyword Fecal transplantation
• dc.subject.keyword Human
• dc.subject.keyword Memory
• dc.subject.keyword Mice
• dc.subject.keyword Microbiome
• dc.title Caudovirales bacteriophages are associated with improved executive function and memory in flies, mice, and humans
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion