Metabolic Architecture of the Deep Ocean Microbiome

Abstract

§ Equal contribution to this work. *Correspondence to: sacinas@icm.csic.es; Tel (+34) 93 230 8565; Fax (+34) 93 230 95 55. AbstractThe deep sea, the largest compartment of the ocean, is an essential component of the Earth system, but the functional exploration of its microbial communities lags far behind that of other marine realms. Here we analyze 58 bathypelagic microbial metagenomes from the Atlantic, Indian, and Pacific Oceans in an unprecedented sampling effort from the Malaspina Global Expedition, to resolve the metabolic architecture of the deep ocean microbiome. The Malaspina Deep-Sea Gene Collection, 71% of which consists of novel genes, reveals a strong dichotomy between the functional traits of free-living and particle-attached microorganisms, and shows relatively patchy composition challenging the paradigm of a uniform dark ocean ecosystem. Metagenome Assembled Genomes uncovered 11 potential new phyla, establishing references for deep ocean microbial taxa, and revealed mixotrophy to be a widespread trophic strategy in the deep ocean. These results expand our understanding of the functional diversity, metabolic versatility, and carbon cycling in the largest ecosystem on Earth. One Sentence Summary:A whole community genomic survey of the deep microbiome sheds light on the microbial and functional diversity of the dark ocean.Main Text.

Major imprint of surface plankton on deep ocean prokaryotic structure and activity

“…Our recent finding that sinking particles transport prokaryotes from surface to bathypelagic waters (Mestre et al., 2018) suggests that the influence of epipelagic processes on the deep‐sea microbiome extends beyond the delivery of photosynthetically‐produced material (Arístegui et al, 2009; Herndl & Reinthaler, 2013). However, most recent efforts to characterize the global biogeography or the functional potential of bathypelagic microorganisms have focused exclusively on the bathypelagic layer itself, disregarding the potential connectivity with surface stocks or processes (Acinas et al, 2019; Pernice et al., 2015, 2016; Salazar, Cornejo‐Castillo, Benítez‐Barrios, et al, 2015; Salazar, Cornejo‐Castillo, Borrull, et al, 2015). Here, we show a link between the spatial structure of bathypelagic prokaryotic assemblages and planktonic community composition in the overlying surface waters.…”

“…On the other hand, some bathypelagic prokaryotes may be less directly (or less immediately) connected to surface processes if relying on metabolisms involving inorganic carbon fixation (Acinas et al, 2019; Pachiadaki et al., 2017; Swan et al., 2011), on organic carbon produced in situ by other autotrophs (Bayer et al., 2019), or on recalcitrant carbon of older origin (Landry et al, 2017). Interestingly, we identified a fraction of bathypelagic endemic taxa that were not detected in any sunlit water, and that were less strongly related to surface biotic conditions than the surface‐related component; local factors such as temperature and the proportions of the FDOM components C1 and C3 in bathypelagic waters appeared as the most important drivers of the taxonomic structure of this endemic component of deep sea prokaryotic assemblages.…”

Sequencing effort dictates gene discovery in marine microbial metagenomes

“…The recent sequencing of 60 deep‐sea (~4 km depth) metagenomes sampled by the Malaspina Circumnavigation Expedition (Acinas et al ., 2019; Supplementary Data 4) supported a yield 10‐fold larger than that produced by Tara Ocean (5.7 vs. 55.4 million unique genes Tbp −1 ) despite the 50‐fold larger sequencing effort applied in the Tara Ocean program (Table 1; Supplementary Data 2). The yield of Tara Ocean is, however, similar to that retrieved from a collection of 610 marine metagenomes sampled across space (5–1000 m) and time (Supplementary Data 5), encompassing samples from the GEOTRACES cruises (2010–2011) and the time‐series data collection from the Station ALOHA and BATS (Biller et al ., 2018).…”

Hiding in Plain Sight: The Globally Distributed Bacterial Candidate Phylum PAUC34f

“…Recruitment against Poribacteria and Latescibacteria SAGs and MAGs was also performed for comparative analyses ( Table 1). Of the 184 metagenomes used ( Supplementary Table S3), 78 were from the Tara Oceans Expedition (Pesant et al, 2015), and additional marine metagenomes were from the Malaspina (Duarte, 2015;Acinas et al, 2019) and other oceanographic expeditions, covering all oceanic realms (from the euphotic to the abyssopelagic zone), including oxygen minimum zones (Tsementzi et al, 2016). Additionally, we included metagenomes from environments where PAUC34f SAGs and MAGs have been identified, including the NC-GWE-OV-2 aquifer, Lake Baikal, and sponges.…”

“…We also explored the potential role of particles as a niche for the oceanic PAUC34f. The metagenomic datasets from Tara and Malaspina were generated from filters of different pore sizes, thus enriched in the "free-living" microbial fraction (0.2-0.8 µm for Malaspina; 0.2-0.8 µm or 0.2-3 µm for Tara) or enriched in the "particle-associated" fraction (>0.8 µm for Malaspina; >3 µm for Tara) (Pesant et al, 2015;Acinas et al, 2019). However, only Malaspina data included size-fractionated dark ocean metagenomes (Supplementary Table S4); in these data, PAUC34f 's relative recruitment from the free-living fraction was on average seven times higher compared to the particleassociated fraction (Supplementary Figure S1).…”