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

Silvia G. Acinas, Pablo Sánchez, Guillem Salazar, Fran 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 S. Alam, Allan Kamau, Chris Bowler, Jeroen Raes, Stéphane Pesant, Peer Bork, Susana Agustí, Takashi Gojobori, Dolors Vaqué, Matthew B. Sullivan, Carlos Pedrós-Alió, Ramon Massana, Carlos M. Duarte, Josep M. Gasol

2021, 4, 604.

Abstract

Abstract The 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 H 2 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.