skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Communications Biology
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [1]; ORCiD logo [1];  [5]; ORCiD logo [5];  [6]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [9]; ORCiD logo [10]; ORCiD logo [11]; ORCiD logo [12]; ORCiD logo [12]; ORCiD logo [13];  [14];  [15] more »; ORCiD logo [16]; ORCiD logo [12];  [12]; ORCiD logo [1];  [17]; ORCiD logo [1]; ORCiD logo [12]; ORCiD logo [18];  [19] « less
  1. Inst. of Marine Sciences (ICM), Barcelona (Spain)
  2. Inst. of Marine Sciences (ICM), Barcelona (Spain); ETH Zurich (Switzerland)
  3. Inst. of Marine Sciences (ICM), Barcelona (Spain); Univ. of California, Santa Cruz, CA (United States)
  4. Inst. of Marine Sciences (ICM), Barcelona (Spain); Univ. de Las Palmas de Gran Canaria, Gran Marta (Sebastian)
  5. ETH Zurich (Switzerland)
  6. Univ. de Toulon, Marseille (France)
  7. Kyoto Univ., Uji (Japan)
  8. Univ. libre de Bruxelles (ULB), Brussels (Belgium); Interuniversity Inst. for Bioinformatics in Brussels (Belgium)
  9. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); The Ohio State Univ., Columbus, OH (United States)
  10. Univ. of La Laguna (Spain)
  11. Spanish Institute of Oceanography (IEO), Santa Cruz de Tenerife (Spain)
  12. King Abdullah Univ. of Science and Technology (KAUST), Thuwal (Saudi Arabia)
  13. Univ. PSL, Paris (France); Research Federation for the study of Global Ocean Systems Ecology and Evolution, Paris (France)
  14. Univ. of Leuven (Belgium); VIB Center for Microbiology, Leuven (Belgium)
  15. European Molecular Biology Lab., European Bioinformatics Institute (EMBL-EBI), Cambridge (United Kingdom); Univ. of Bremen (Germany)
  16. European Molecular Biology Lab., Heidelberg (Germany)
  17. Centro Nacional de Biotecnología (CNB), Madrid (Spain)
  18. Inst. of Marine Sciences (ICM), Barcelona (Spain); Edith Cowan Univ., Joondalup (Australia)
  19. The Ohio State Univ., Columbus, OH (United States)

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.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1826332
Journal Information:
Communications Biology, Vol. 4, Issue 1; ISSN 2399-3642
Publisher:
Springer NatureCopyright Statement
Country of Publication:
United States
Language:
English

References (118)

Major imprint of surface plankton on deep ocean prokaryotic structure and activity journal May 2020
Mesoscale eddies: hotspots of prokaryotic activity and differential community structure in the ocean journal April 2010
Contribution of Bicarbonate Assimilation to Carbon Pool Dynamics in the Deep Mediterranean Sea and Cultivation of Actively Nitrifying and CO2-Fixing Bathypelagic Prokaryotic Consortia journal January 2018
A new method for non-parametric multivariate analysis of variance journal February 2001
Microbial oceanography of the dark ocean's pelagic realm journal June 2009
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea journal August 2017
Oxidation of Inorganic Sulfur Compounds by Obligately Organotrophic Bacteria journal November 2003
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival journal July 2019
Citreicella thiooxidans gen. nov., sp. nov., a novel lithoheterotrophic sulfur-oxidizing bacterium from the Black Sea journal October 2005
Major role of bacteria in biogeochemical fluxes in the ocean's interior journal March 1988
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic journal September 2015
Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus journal December 2009
Episodic organic carbon fluxes from surface ocean to abyssal depths during long-term monitoring in NE Pacific journal November 2018
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities journal January 2015
Physiological, Ecological, and Phylogenetic Characterization of Stappia , a Marine CO-Oxidizing Bacterial Genus journal February 2007
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches journal November 2014
Influence of nutrients and currents on the genomic composition of microbes across an upwelling mosaic journal January 2012
The role of subduction and gravitational sinking in particle export, carbon sequestration, and the remineralization length scale in the California Current Ecosystem: Subduction and sinking particle export in the CCE journal July 2017
Particle-association lifestyle is a phylogenetically conserved trait in bathypelagic prokaryotes journal November 2015
Fast and sensitive protein alignment using DIAMOND journal November 2014
The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy journal November 2012
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria journal December 2012
Metagenomic Evidence for H2 Oxidation and H2 Production by Serpentinite-Hosted Subsurface Microbial Communities journal January 2012
Phylogenetic Analysis of Particle-Attached and Free-Living Bacterial Communities in the Columbia River, Its Estuary, and the Adjacent Coastal Ocean journal July 1999
Ketobacter alkanivorans gen. nov., sp. nov., an n-alkane-degrading bacterium isolated from seawater journal July 2018
Prokka: rapid prokaryotic genome annotation journal March 2014
The biomass distribution on Earth journal May 2018
Role for urea in nitrification by polar marine Archaea journal October 2012
Changing perspectives in marine nitrogen fixation journal May 2020
Sinking particles promote vertical connectivity in the ocean microbiome journal July 2018
The NCBI Taxonomy database journal December 2011
Nitrogenase Gene Amplicons from Global Marine Surface Waters Are Dominated by Genes of Non-Cyanobacteria journal April 2011
Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics journal December 2017
Beyond the Calvin Cycle: Autotrophic Carbon Fixation in the Ocean journal January 2011
Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior journal January 2006
Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic journal September 2006
Structure and function of the global ocean microbiome journal May 2015
Archaeal nitrification in the ocean journal August 2006
Isolation and Characterization of Novosphingobium sp. Strain MT1, a Dominant Polychlorophenol-Degrading Strain in a Groundwater Bioremediation System journal January 2002
Life with Carbon Monoxide journal January 2004
Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities: Using journal September 2013
Not All Particles Are Equal: The Selective Enrichment of Particle-Associated Bacteria from the Mediterranean Sea journal June 2016
Global diversity and biogeography of deep-sea pelagic prokaryotes journal August 2015
Major role of nitrite-oxidizing bacteria in dark ocean carbon fixation journal November 2017
Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight journal April 2011
Isolation of an autotrophic ammonia-oxidizing marine archaeon journal September 2005
Characteristics of diazotrophs in surface to abyssopelagic waters of the Sargasso Sea journal January 2007
An assessment of the use of sediment traps for estimating upper ocean particle fluxes journal May 2007
Interactive Tree Of Life (iTOL) v4: recent updates and new developments journal April 2019
KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold journal November 2019
Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea) journal January 2011
Structure of cytochrome c nitrite reductase journal July 1999
Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean journal September 2011
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix journal April 2009
Microbial control of the dark end of the biological pump journal August 2013
Ballast, sinking velocity, and apparent diffusivity within marine snow and zooplankton fecal pellets: Implications for substrate turnover by attached bacteria journal September 2008
Diversity of total and active free-living vs. particle-attached bacteria in the euphotic zone of the NW Mediterranean Sea journal October 2009
Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes journal April 2018
The complete genome sequence and analysis of a plasmid-bearing myxobacterial strain Myxococcus fulvus 124B02 (M 206081) journal January 2016
SAR202 Genomes from the Dark Ocean Predict Pathways for the Oxidation of Recalcitrant Dissolved Organic Matter journal April 2017
The enigmatic SAR202 cluster up close: shedding light on a globally distributed dark ocean lineage involved in sulfur cycling journal December 2017
Size-fraction partitioning of community gene transcription and nitrogen metabolism in a marine oxygen minimum zone journal April 2015
Diverse diazotrophs are present on sinking particles in the North Pacific Subtropical Gyre journal August 2018
Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships journal June 2007
Contribution of Archaea to Total Prokaryotic Production in the Deep Atlantic Ocean journal May 2005
Prokaryotic extracellular enzymatic activity in relation to biomass production and respiration in the meso- and bathypelagic waters of the (sub)tropical Atlantic journal August 2009
Dissolved Organic Carbon Support of Respiration in the Dark Ocean journal December 2002
Novosphingobium indicum sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from a deep-sea environment journal July 2009
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences journal May 2006
Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution journal January 2009
Multi-faceted particle pumps drive carbon sequestration in the ocean journal April 2019
Seafaring in the 21St Century: The Malaspina 2010 Circumnavigation Expedition journal January 2015
Global genetic capacity for mixotrophy in marine picocyanobacteria journal May 2016
CO Dehydrogenase Genes Found in Metagenomic Fosmid Clones from the Deep Mediterranean Sea journal October 2009
Patterns and ecological drivers of ocean viral communities journal May 2015
Global niche of marine anaerobic metabolisms expanded by particle microenvironments journal March 2018
Eddy-driven subduction exports particulate organic carbon from the spring bloom journal March 2015
Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic’s interior journal August 2010
Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms journal January 2002
Metagenomics of the Deep Mediterranean, a Warm Bathypelagic Habitat journal September 2007
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses journal September 2016
CAP3: A DNA Sequence Assembly Program journal September 1999
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont journal May 2002
MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices journal June 2016
Search and clustering orders of magnitude faster than BLAST journal August 2010
Significance of non-sinking particulate organic carbon and dark CO 2 fixation to heterotrophic carbon demand in the mesopelagic northeast Atlantic: DARK CO 2 FIXATION AND C DEMAND journal May 2010
Respiration in the open ocean journal November 2002
Expanded microbial genome coverage and improved protein family annotation in the COG database journal November 2014
Transcriptional control, translation and function of the products of the five open reading frames of the Escherichia coli nir operon journal October 1992
Decoupling function and taxonomy in the global ocean microbiome journal September 2016
290 metagenome-assembled genomes from the Mediterranean Sea: a resource for marine microbiology journal January 2017
The Pfam protein families database in 2019 journal October 2018
Diversity of Myxobacteria—We Only See the Tip of the Iceberg journal August 2018
Novosphingobium nitrogenifigens sp. nov., a polyhydroxyalkanoate-accumulating diazotroph isolated from a New Zealand pulp and paper wastewater journal November 2007
The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific journal March 2007
Accelerated Profile HMM Searches journal October 2011
Large variability of bathypelagic microbial eukaryotic communities across the world’s oceans journal October 2015
Fast gapped-read alignment with Bowtie 2 journal March 2012
Functional assignment of multiple catabolic pathways for d-apiose journal June 2018
Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean journal June 2020
Lateral Gene Transfer Shapes the Distribution of RuBisCO among Candidate Phyla Radiation Bacteria and DPANN Archaea journal December 2018
Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes journal April 2013
Complete Genome of the Starch-Degrading Myxobacteria Sandaracinus amylolyticus DSM 53668 T journal June 2016
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal January 2011
High bicarbonate assimilation in the dark by Arctic bacteria journal June 2010
Chasing after Non-cyanobacterial Nitrogen Fixation in Marine Pelagic Environments journal September 2017
How microbes survive in the open ocean journal August 2017
Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump journal July 2015
Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome journal November 2019
The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans journal January 2018
Substantial energy input to the mesopelagic ecosystem from the seasonal mixed-layer pump journal September 2016
Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes journal June 2018
The Sequence Alignment/Map format and SAMtools journal June 2009
Bacterial species may exist, metagenomics reveal: Bacterial species may exist journal December 2011