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

Title: Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre

Journal Article · · Frontiers in Microbiology
 [1];  [2];  [3];  [4];  [2]
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Univ. of Hawaii, Honolulu, HI (United States)
  3. Univ. of Hawaii, Honolulu, HI (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  4. Univ. of Hawaii, Honolulu, HI (United States)

Sinking particles mediate the transport of carbon and energy to the deep-sea, yet the specific microbes associated with sedimenting particles in the ocean's interior remain largely uncharacterized. In this study, we used particle interceptor traps (PITs) to assess the nature of particle-associated microbial communities collected at a variety of depths in the North Pacific Subtropical Gyre. Comparative metagenomics was used to assess differences in microbial taxa and functional gene repertoires in PITs containing a preservative (poisoned traps) compared to preservative-free traps where growth was allowed to continue in situ (live traps). Live trap microbial communities shared taxonomic and functional similarities with bacteria previously reported to be enriched in dissolved organic matter (DOM) microcosms (e.g., Alteromonas and Methylophaga), in addition to other particle and eukaryote-associated bacteria (e.g., Flavobacteriales and Pseudoalteromonas). Poisoned trap microbial assemblages were enriched in Vibrio and Campylobacterales likely associated with eukaryotic surfaces and intestinal tracts as symbionts, pathogens, or saprophytes. The functional gene content of microbial assemblages in poisoned traps included a variety of genes involved in virulence, anaerobic metabolism, attachment to chitinaceaous surfaces, and chitin degradation. The presence of chitinaceaous surfaces was also accompanied by the co-existence of bacteria which encoded the capacity to attach to, transport and metabolize chitin and its derivatives. Distinctly different microbial assemblages predominated in live traps, which were largely represented by copiotrophs and eukaryote-associated bacterial communities. Predominant sediment trap-assocaited eukaryotic phyla included Dinoflagellata, Metazoa (mostly copepods), Protalveolata, Retaria, and Stramenopiles. In conclusion, these data indicate the central role of eukaryotic taxa in structuring sinking particle microbial assemblages, as well as the rapid responses of indigenous microbial species in the degradation of marine particulate organic matter (POM) in situ in the ocean's interior.

Research Organization:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Organization:
USDOE; National Science Foundation (NSF)
Grant/Contract Number:
EF0424599; 329108; 3777; 3794; AC52-07NA27344
OSTI ID:
1259661
Alternate ID(s):
OSTI ID: 1418923
Report Number(s):
LLNL-JRNL-735612
Journal Information:
Frontiers in Microbiology, Vol. 6; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 106 works
Citation information provided by
Web of Science

References (106)

Carbon substrate usage by zooplankton-associated bacteria, phytoplankton-associated bacteria, and free-living bacteria under aerobic and anaerobic conditions journal July 2014
Microbial ecology of organic aggregates in aquatic ecosystems journal January 2002
A mannose-sensitive haemagglutinin (MSHA)-like pilus promotes attachment of Pseudoalteromonas tunicata cells to the surface of the green alga Ulva australis journal October 2006
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides journal October 2010
Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level journal January 2014
Impact of warming on phyto-bacterioplankton coupling and bacterial community composition in experimental mesocosms: Temperature impact on phyto-bacterioplankton coupling journal July 2013
Obligate oil-degrading marine bacteria journal June 2007
Fate of polycyclic aromatic hydrocarbons in controlled ecosystem enclosures journal July 1978
Analysis of the Pseudoalteromonas tunicata Genome Reveals Properties of a Surface-Associated Life Style in the Marine Environment journal September 2008
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
Degradation and dissolution properties of photosynthetically-produced phytoplankton lipid materials in early diagenesis journal April 2009
Metabolic strategies of free-living and aggregate-associated bacterial communities inferred from biologic and chemical profiles in the Black Sea suboxic zone journal September 2011
Complete genome sequence of Marinobacter adhaerens type strain (HP15), a diatom-interacting marine microorganism journal September 2010
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal January 2009
Particulate Organic Matter in the Sea: The Composition Conundrum journal January 2004
Influence of nutrients and currents on the genomic composition of microbes across an upwelling mosaic journal January 2012
Planktonic Euryarchaeota are a significant source of archaeal tetraether lipids in the ocean journal June 2014
Detection of V ibrio parahaemolyticus , V ibrio vulnificus and V ibrio cholerae with respect to seasonal fluctuations in temperature and plankton abundance : Abiotic and biotic interactions in journal September 2013
Indigenous ectosymbiotic bacteria associated with diverse hydrothermal vent invertebrates: Indigenous bacteria associated with vent invertebrates journal February 2010
Comparison of free-living, suspended particle, and aggregate-associated Bacterial and Archaeal communities in the Laptev Sea journal September 2009
Chemical and Biological Studies of Particulate Organic Matter in the Ocean journal March 2002
Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea journal August 2010
Adaptive seeds tame genomic sequence comparison journal January 2011
Biodiversity of Vibrios journal September 2004
Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem journal January 2013
Lineage specific gene family enrichment at the microscale in marine systems journal October 2013
Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior journal January 2006
Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations journal November 2012
Bacterial chemolithotrophy in the ocean is associated with sinking particles journal May 1984
Copepod guts as biogeochemical hotspots in the sea: Evidence from microelectrode profiling of Calanus spp journal February 2011
Substrate-Specific Clades of Active Marine Methylotrophs Associated with a Phytoplankton Bloom in a Temperate Coastal Environment journal October 2008
Roseobacticides: Small Molecule Modulators of an Algal-Bacterial Symbiosis journal November 2011
Gamma- and epsilonproteobacterial ectosymbionts of a shallow-water marine worm are related to deep-sea hydrothermal vent ectosymbionts: Ectosymbionts of a marine oligochaete worm journal June 2010
VEGAN, a package of R functions for community ecology journal April 2003
Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the  -Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough journal March 2005
Marine macroalgae: an untapped resource for producing fuels and chemicals journal February 2013
Fluxes of particulate carbon, nitrogen, and phosphorus in the upper water column of the northeast Pacific journal January 1979
Bacterial Reduction of Trimethylamine Oxide journal October 1985
Dynamics of Bacterial Community Composition and Activity during a Mesocosm Diatom Bloom journal February 2000
Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean journal September 2011
Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages journal July 1993
Horizontal and vertical complexity of attached and free-living bacteria of the eastern Mediterranean Sea, determined by 16S rDNA and 16S rRNA fingerprints journal January 2001
The Mannose-Sensitive Hemagglutinin of Vibrio cholerae Promotes Adherence to Zooplankton journal July 2001
Pathogenic Vibrio, Aeromonas and Arcobacter spp. associated with copepods in the Straits of Messina (Italy) journal March 2008
Temporal changes in particle-associated microbial communities after interception by nonlethal sediment traps journal October 2013
Free-living and aggregate-associated Planctomycetes in the Black Sea journal February 2012
Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph journal September 2012
Metapopulation structure of Vibrionaceae among coastal marine invertebrates journal September 2010
Bacterial chitin degradation—mechanisms and ecophysiological strategies journal January 2013
Molecular characterization of dissolved organic matter (DOM): a critical review journal September 2012
Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution journal September 1992
Characterization of the first alginolytic operons in a marine bacterium: from their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides: Emergence and transfer of alginolytic operons journal April 2012
Taxonomic composition of the particle-attached and free-living bacterial assemblages in the Northwest Mediterranean Sea analyzed by pyrosequencing of the 16S rRNA journal May 2013
The Vibrio cholerae chitin utilization program journal February 2004
VERTIGO (VERtical Transport In the Global Ocean): A study of particle sources and flux attenuation in the North Pacific journal July 2008
PANDAseq: paired-end assembler for illumina sequences journal January 2012
<I>In situ</I> effects of selected preservatives on total carbon, nitrogen and metals collected in sediment traps journal May 1984
VERTEX: carbon cycling in the northeast Pacific journal February 1987
NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions journal October 2012
Note: Sulfurospirillum barnesii sp. nov. and Sulfurospirillum arsenophilum sp. nov., new members of the Sulfurospirillum clade of the  -Proteobacteria journal July 1999
Degradation and dissolution of zooplanktonic organic matter and lipids in early diagenesis journal December 2011
Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone journal September 2013
Rheinheimera perlucida sp. nov., a marine bacterium of the Gammaproteobacteria isolated from surface water of the central Baltic Sea journal September 2006
Changes in Bacterioplankton Composition under Different Phytoplankton Regimens journal November 2004
Population dynamics of Cytophaga-Flavobacteria during marine phytoplankton blooms analyzed by real-time quantitative PCR journal January 2005
Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment: Microbial diversity in the Puerto Rico Trench journal November 2010
Siderophore-Based Iron Acquisition and Pathogen Control journal September 2007
dbCAN: a web resource for automated carbohydrate-active enzyme annotation journal May 2012
The Genome of the Alga-Associated Marine Flavobacterium Formosa agariphila KMM 3901 T Reveals a Broad Potential for Degradation of Algal Polysaccharides journal August 2013
The PAH and organic content of sediment particle size fractions journal May 1990
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data journal April 2013
One Carbon Metabolism in SAR11 Pelagic Marine Bacteria journal August 2011
Porticoccus hydrocarbonoclasticus sp. nov., an Aromatic Hydrocarbon-Degrading Bacterium Identified in Laboratory Cultures of Marine Phytoplankton journal December 2011
Putative virulence genes in Moritella viscosa: Activity during in vitro inoculation and in vivo infection journal June 2011
Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis, and Thalassiosira weissflogii) incubated under various conditions in the lab journal January 1999
Vertical flux of particles in the ocean journal July 1975
Anaerobic respiratory growth of Vibrio harveyi, Vibrio fischeri and Photobacterium leiognathi with trimethylamine N-oxide, nitrate and fumarate: ecological implications journal August 2000
Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions journal January 2002
Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii journal September 2010
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data journal October 2012
Biogeochemical significance of attached and free-living bacteria and the flux of particles in the NE Atlantic Ocean journal January 1994
Accelerated Profile HMM Searches journal October 2011
Planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda: abundance, biomass and vertical flux journal January 1995
Whole genome analysis of the marine Bacteroidetes 'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter journal December 2006
Role of macroscopic particles in deep-sea oxygen consumption journal April 2010
Transformations of biogenic particulates from the pelagic to the deep ocean realm journal November 1999
Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom journal May 2012
The versatile ε-proteobacteria: key players in sulphidic habitats journal May 2006
Small Phytoplankton and Carbon Export from the Surface Ocean journal February 2007
Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I journal February 2007
The flux of bio- and lithogenic material associated with sinking particles in the mesopelagic “twilight zone” of the northwest and North Central Pacific Ocean journal July 2008
Particulate organic carbon fluxes to the ocean interior and factors controlling the biological pump: A synthesis of global sediment trap programs since 1983 journal March 2008
Bacterial chitinases and chitin-binding proteins as virulence factors journal March 2013
Identifying biologically relevant differences between metagenomic communities journal February 2010
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Phylogenetic Analysis of Particle-Attached and Free-Living Bacterial Communities in the Columbia River, Its Estuary, and the Adjacent Coastal Ocean journal July 1999
Dynamics of Bacterial Community Composition and Activity during a Mesocosm Diatom Bloom journal May 2000
Characterization and functional analysis of phytoene synthase gene family in tobacco journal January 2021
Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the ε-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough journal September 2005
Porticoccus hydrocarbonoclasticus sp. nov., an Aromatic Hydrocarbon-Degrading Bacterium Identified in Laboratory Cultures of Marine Phytoplankton text January 2012
Physiological aspects of chitin catabolism in marine bacteria journal December 1999
Heavy metals in particulate matter and sediments in the southern Barcelona sedimentation system (North-western Mediterranean) journal January 1999
CXCR4 signaling directs Igk recombination and the molecular mechanisms of late B lymphopoiesis journal September 2019
Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes journal February 2020
Particulate Organic Matter in the Sea: The Composition Conundrum journal December 2004

Cited By (39)

Linking biochemical properties of particles to particle-attached and free-living bacterial community structure along the particle density gradient from freshwater to open ocean: Linking POM to Particle-Attached and Free-Living Bacteria journal August 2016
Hard and soft plastic resin embedding for single-cell element uptake investigations of marine-snow-associated microorganisms using nano-scale secondary ion mass spectrometry: NanoSIMS of sectioned marine snow samples journal July 2018
Ecogenomics of Deep-Ocean Microbial Bathytypes book March 2017
Comparison of community structures between particle-associated and free-living prokaryotes in tropical and subtropical Pacific Ocean surface waters journal January 2017
Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean journal May 2017
Plankton networks driving carbon export in the oligotrophic ocean journal February 2016
Coordinated gene expression between Trichodesmium and its microbiome over day–night cycles in the North Pacific Subtropical Gyre journal January 2018
Diverse diazotrophs are present on sinking particles in the North Pacific Subtropical Gyre journal August 2018
High contribution of Rhizaria (Radiolaria) to vertical export in the California Current Ecosystem revealed by DNA metabarcoding journal December 2018
Phage-specific metabolic reprogramming of virocells journal January 2020
Understanding microbial community dynamics to improve optimal microbiome selection journal June 2019
Contrasting seasonal drivers of virus abundance and production in the North Pacific Ocean journal September 2017
Vertically distinct microbial communities in the Mariana and Kermadec trenches journal April 2018
Particle-Associated Differ from Free-Living Bacteria in Surface Waters of the Baltic Sea journal December 2015
Identification of Associations between Bacterioplankton and Photosynthetic Picoeukaryotes in Coastal Waters journal March 2016
Co-occurrence Analysis of Microbial Taxa in the Atlantic Ocean Reveals High Connectivity in the Free-Living Bacterioplankton journal May 2016
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept journal July 2017
Bacterial Succession on Sinking Particles in the Ocean's Interior journal November 2017
In Situ Diazotroph Population Dynamics Under Different Resource Ratios in the North Pacific Subtropical Gyre journal July 2018
A missing link in the estuarine nitrogen cycle?: Coupled nitrification-denitrification mediated by suspended particulate matter journal February 2018
Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean journal October 2015
Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean journal May 2019
Micro-scale ecology regulates particulate organic matter turnover in model marine microbial communities posted_content January 2018
Prokaryotic niche partitioning between suspended and sinking marine particles journal October 2018
Microbial Communities in the East and West Fram Strait During Sea Ice Melting Season journal November 2018
Changes in Carbon Oxidation State of Metagenomes Along Geochemical Redox Gradients journal February 2019
Motility drives bacterial encounter with particles responsible for carbon export throughout the ocean text January 2019
Eukaryotic microbes, principally fungi and labyrinthulomycetes, dominate biomass on bathypelagic marine snow journal September 2016
In situ imaging reveals the biomass of giant protists in the global ocean journal April 2016
Microscale ecology regulates particulate organic matter turnover in model marine microbial communities text January 2018
Las parroquias en los dominios monásticos castellanos en la Baja Edad Media y principios de la Moderna: San Zoilo de Carrión y San Román de Entrepeñas (siglos XIV-XVI) journal December 2017
Metabolite composition of sinking particles differs from surface suspended particles across a latitudinal transect in the South Atlantic journal July 2019
Motility drives bacterial encounter with particles responsible for carbon export throughout the ocean journal July 2019
Paired high-throughput, in-situ imaging and high-throughput sequencing illuminate acantharian abundance and vertical distribution journal February 2020
Six Pseudoalteromonas Strains Isolated from Surface Waters of Kabeltonne, Offshore Helgoland, North Sea journal February 2016
Seasonal Succession Leads to Habitat-Dependent Differentiation in Ribosomal RNA:DNA Ratios among Freshwater Lake Bacteria journal April 2016
Microbial Community Response to Terrestrially Derived Dissolved Organic Matter in the Coastal Arctic journal June 2017
Microbiome of Trichodesmium Colonies from the North Pacific Subtropical Gyre journal July 2017
Persistent Core Populations Shape the Microbiome Throughout the Water Column in the North Pacific Subtropical Gyre journal October 2019