Deep ocean metagenomes provide insight into the metabolic architecture of bathypelagic microbial communities

Silvia G. Acinas, Pablo Sánchez, Guillem Salazar, Francisco M. Cornejo-Castillo, Marta Sebastián, Ramiro Logares, Marta Royo-Llonch, Lucas Paoli, Shinichi Sunagawa, Pascal Hingamp, Hiroyuki Ogata, Gipsi Lima-Mendez, Simon Roux, José M. González, Jesús M. Arrieta, Intikhab Alam, Allan Kamau, Chris Bowler, Jeroen Raes, Stéphane PesantPeer Bork, Susana Agusti, Takashi Gojobori, Dolors Vaqué, Matthew B. Sullivan, Carlos Pedrós-Alió, Ramon Massana, Carlos M. Duarte, Josep M. Gasol

Research output: Contribution to journalArticlepeer-review

76 Scopus citations

Abstract

AbstractThe deep sea, the largest ocean’s compartment, drives planetary-scale biogeochemical cycling. Yet, the functional exploration of its microbial communities lags far behind other environments. Here we analyze 58 metagenomes from tropical and subtropical deep oceans to generate the Malaspina Gene Database. Free-living or particle-attached lifestyles drive functional differences in bathypelagic prokaryotic communities, regardless of their biogeography. Ammonia and CO oxidation pathways are enriched in the free-living microbial communities and dissimilatory nitrate reduction to ammonium and H2 oxidation pathways in the particle-attached, while the Calvin Benson-Bassham cycle is the most prevalent inorganic carbon fixation pathway in both size fractions. Reconstruction of the Malaspina Deep Metagenome-Assembled Genomes reveals unique non-cyanobacterial diazotrophic bacteria and chemolithoautotrophic prokaryotes. The widespread potential to grow both autotrophically and heterotrophically suggests that mixotrophy is an ecologically relevant trait in the deep ocean. These results expand our understanding of the functional microbial structure and metabolic capabilities of the largest Earth aquatic ecosystem.
Original languageEnglish (US)
JournalCommunications Biology
Volume4
Issue number1
DOIs
StatePublished - May 21 2021

Bibliographical note

KAUST Repository Item: Exported on 2021-05-25
Acknowledged KAUST grant number(s): OSR #3362
Acknowledgements: We thank the R/V Hespérides captain and crew, the chief scientists in Malaspina expedition legs, and all project participants for their help in making this project possible. This work was funded by the Spanish Ministry of Economy and Competitiveness (MINECO) through the Consolider-Ingenio program (Malaspina 2010 Expedition, ref. CSD2008-00077). The sequencing of 58 bathypelagic metagenomes was done by the U.S. Department of Energy Joint Genome Institute, supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02 05CH11231 to SGA (CSP 612 “Microbial metagenomics and transcriptomics from a global deep-ocean expedition”). Additional funding was provided by the project MAGGY (CTM2017-87736-R) to S.G.A. from the Spanish Ministry of Economy and Competitiveness, Grup de Recerca 2017SGR/1568 from Generalitat de Catalunya, and King Abdullah University of Science and Technology (KAUST) under contract OSR #3362 and by funding of the EMFF Program of the European Union (MERCLUB project, Grant Agreement 863584). The ICM researchers have had the institutional support of the “Severo Ochoa Centre of Excellence” accreditation (CEX2019-000928-S). High-Performance computing analyses were run at the Marine Bioinformatics Service (MARBITS, https://marbits.icm.csic.es) of the Institut de Ciències del Mar (ICM-CSIC), Barcelona, Supercomputing Center (Grant BCV-2013-2-0001) and KAUST’s Ibex HPC. We thank Shook Studio for assistance with figure design and implementation and the anonymous reviewers for their comments to improve this manuscript. This paper is dedicated to the memory of Professor Vladimir B. Bajic, 2019.

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