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

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

doi:10.1038/s42003-021-02112-2

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 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.

Highlights

The deep sea, the largest ocean’s compartment, drives planetary-scale biogeochemical cycling
The high respiratory activity measured in the dark ocean is difficult to reconcile with the rates of supply of organic carbon produced in the photic layer[3,4,5,6,7], suggesting the existence of other sources of carbon, such as potentially nonsinking POC and in situ production by autochthonous microbial chemolithoautotrophs[8]
Experimental rate measurements and bulk biogeochemical estimates agree with findings using single-cell genomics that ubiquitous bacterial lineages have the potential for inorganic carbon fixation[17,18], suggesting that chemolithoautotrophy may be a substantial contributor to deep-sea metabolism and may play a greater role in the global ocean carbon cycle than previously thought

Summary

Introduction

The deep sea, the largest ocean’s compartment, drives planetary-scale biogeochemical cycling. 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. Besides living in permanent darkness, deep-ocean organisms have to cope and adapt to the high pressure and low temperature that characterize this ecosystem This fascinating habitat represents one of the largest biomes on Earth, mostly occupied by bacteria and archaea that play a pivotal role in biogeochemical cycles on a planetary scale[1,2]. Despite the potential importance of organic carbon derived from chemolithoautotrophy, particles likely represent the main source of reduced C to the deep ocean and constitute important hotspots of microbial activity that fuel the dark ocean food web[7]. We constructed the Malaspina Deep Metagenome-Assembled Genomes (MDeep-MAGs) catalog to explore the metabolic potential of the deep-sea microbiome

Methods

Results

Conclusion