Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean.
ABSTRACT: Sinking particles are a critical conduit for the export of organic material from surface waters to the deep ocean. Despite their importance in oceanic carbon cycling and export, little is known about the biotic composition, origins, and variability of sinking particles reaching abyssal depths. Here, we analyzed particle-associated nucleic acids captured and preserved in sediment traps at 4,000-m depth in the North Pacific Subtropical Gyre. Over the 9-month time-series, Bacteria dominated both the rRNA-gene and rRNA pools, followed by eukaryotes (protists and animals) and trace amounts of Archaea. Deep-sea piezophile-like Gammaproteobacteria, along with Epsilonproteobacteria, comprised >80% of the bacterial inventory. Protists (mostly Rhizaria, Syndinales, and ciliates) and metazoa (predominantly pelagic mollusks and cnidarians) were the most common sinking particle-associated eukaryotes. Some near-surface water-derived eukaryotes, especially Foraminifera, Radiolaria, and pteropods, varied greatly in their abundance patterns, presumably due to sporadic export events. The dominance of piezophile-like Gammaproteobacteria and Epsilonproteobacteria, along with the prevalence of their nitrogen cycling-associated gene transcripts, suggested a central role for these bacteria in the mineralization and biogeochemical transformation of sinking particulate organic matter in the deep ocean. Our data also reflected several different modes of particle export dynamics, including summer export, more stochastic inputs from the upper water column by protists and pteropods, and contributions from sinking mid- and deep-water organisms. In total, our observations revealed the variable and heterogeneous biological origins and microbial activities of sinking particles that connect their downward transport, transformation, and degradation to deep-sea biogeochemical processes.
Project description:Two mooring arrays carrying sediment traps were deployed from September 2011 to August 2012 at ?83°N on each side of the Gakkel Ridge in the Nansen and Amundsen Basins to measure downward particle flux below the euphotic zone (approx. 250?m) and approximately 150?m above seafloor at approximately 3500 and 4000?m depth, respectively. In a region that still experiences nearly complete ice cover throughout the year, export fluxes of total particulate matter (TPM), particulate organic carbon (POC), particulate nitrogen (PN), biogenic matter, lithogenic matter, biogenic particulate silica (bPSi), calcium carbonate (CaCO3), protists and biomarkers only slightly decreased with depth. Seasonal variations of particulate matter fluxes were similar on both sides of the Gakkel Ridge. Somewhat higher export rates in the Amundsen Basin and differences in the composition of the sinking TPM and bPSi on each side of the Gakkel Ridge probably reflected the influence of the Lena River/Transpolar Drift in the Amundsen Basin and the influence of Atlantic water in the Nansen Basin. Low variations in particle export with depth revealed a limited influence of lateral advection in the deep barren Eurasian Basin. This article is part of the theme issue 'The changing Arctic Ocean: consequences for biological communities, biogeochemical processes and ecosystem functioning'.
Project description:Enhanced vertical carbon transport (gravitational sinking and subduction) at mesoscale ocean fronts may explain the demonstrated imbalance of new production and sinking particle export in coastal upwelling ecosystems. Based on flux assessments from 238U:234Th disequilibrium and sediment traps, we found 2 to 3 times higher rates of gravitational particle export near a deep-water front (305 mg C⋅m-2⋅d-1) compared with adjacent water or to mean (nonfrontal) regional conditions. Elevated particle flux at the front was mechanistically linked to Fe-stressed diatoms and high mesozooplankton fecal pellet production. Using a data assimilative regional ocean model fit to measured conditions, we estimate that an additional ∼225 mg C⋅m-2⋅d-1 was exported as subduction of particle-rich water at the front, highlighting a transport mechanism that is not captured by sediment traps and is poorly quantified by most models and in situ measurements. Mesoscale fronts may be responsible for over a quarter of total organic carbon sequestration in the California Current and other coastal upwelling ecosystems.
Project description:Macroscopic particles (>500 mum), including marine snow, large migrating zooplankton, and their fast-sinking fecal pellets, represent primary vehicles of organic carbon flux from the surface to the deep sea. In contrast, freely suspended microscopic particles such as bacteria and protists do not sink, and they contribute the largest portion of metabolism in the upper ocean. In bathy- and abyssopelagic layers of the ocean (2,000-6,000 m), however, microscopic particles may not dominate oxygen consumption. In a section across the tropical Atlantic, we show that macroscopic particle peaks occurred frequently in the deep sea, whereas microscopic particles were barely detectable. In 10 of 17 deep-sea profiles (>2,000 m depth), macroscopic particle abundances were more strongly cross-correlated with oxygen deficits than microscopic particles, suggesting that biomass bound to large particles dominates overall deep-sea metabolism.
Project description:The sinking of organic particles formed in the photic layer is a main vector of carbon export into the deep ocean. Although sinking particles are heavily colonized by microbes, so far it has not been explored whether this process plays a role in transferring prokaryotic diversity from surface to deep oceanic layers. Using Illumina sequencing of the 16S rRNA gene, we explore here the vertical connectivity of the ocean microbiome by characterizing marine prokaryotic communities associated with five different size fractions and examining their compositional variability from surface down to 4,000 m across eight stations sampled in the Atlantic, Pacific, and Indian Oceans during the Malaspina 2010 Expedition. Our results show that the most abundant prokaryotes in the deep ocean are also present in surface waters. This vertical community connectivity seems to occur predominantly through the largest particles because communities in the largest size fractions showed the highest taxonomic similarity throughout the water column, whereas free-living communities were more isolated vertically. Our results further suggest that particle colonization processes occurring in surface waters determine to some extent the composition and biogeography of bathypelagic communities. Overall, we postulate that sinking particles function as vectors that inoculate viable particle-attached surface microbes into the deep-sea realm, determining to a considerable extent the structure, functioning, and biogeography of deep ocean communities.
Project description:Marine planktonic organisms that undertake active vertical migrations over their life cycle are important contributors to downward particle flux in the oceans. Acantharia, globally distributed heterotrophic protists that are unique in building skeletons of celestite (strontium sulfate), can produce reproductive cysts covered by a heavy mineral shell that sink rapidly from surface to deep waters. We combined phylogenetic and biogeochemical analyses to explore the ecological and biogeochemical significance of this reproductive strategy. Phylogenetic analysis of the 18S and 28S rRNA genes of different cyst morphotypes collected in different oceans indicated that cyst-forming Acantharia belong to three early diverging and essentially non symbiotic clades from the orders Chaunacanthida and Holacanthida. Environmental high-throughput V9 tag sequences and clone libraries of the 18S rRNA showed that the three clades are widely distributed in the Indian, Atlantic and Pacific Oceans at different latitudes, but appear prominent in regions of higher primary productivity. Moreover, sequences of cyst-forming Acantharia were distributed evenly in both the photic and mesopelagic zone, a vertical distribution that we attribute to their life cycle where flagellated swarmers are released in deep waters from sinking cysts. Bathypelagic sediment traps in the subantarctic and oligotrophic subtropical Atlantic Ocean showed that downward flux of Acantharia was only large at high-latitudes and during a phytoplankton bloom. Their contribution to the total monthly particulate organic matter flux can represent up to 3%. High organic carbon export in cold waters would be a putative nutritional source for juveniles ascending in the water column. This study improves our understanding of the life cycle and biogeochemical contribution of Acantharia, and brings new insights into a remarkable reproductive strategy in marine protists.
Project description:The biological carbon pump exports carbon fixed by photosynthesis out of the surface ocean and transfers it to the deep, mostly in the form of sinking particles. Despite the importance of the pump in regulating the air-sea CO2 balance, the magnitude of global carbon export remains unclear, as do its controlling mechanisms. A possible sinking flux of carbon to the mesopelagic zone may be via the mixed-layer pump: a seasonal net detrainment of particulate organic carbon (POC)-rich surface waters, caused by sequential deepening and shoaling of the mixed layer. In this study, we present a full year of daily small-particle POC concentrations derived from glider optical backscatter data, to study export variability at the Porcupine Abyssal Plain (PAP) sustained observatory in the Northeast Atlantic. We observe a strong seasonality in small-particle transfer efficiency, with a maximum in winter and early spring. By calculating daily POC export driven by mixed-layer variations, we find that the mixed-layer pump supplies an annual flux of at least 3.0 ± 0.9 g POC·m-2·year-1 to the mesopelagic zone, contributing between 5% and 25% of the total annual export flux and likely contributing to closing a gap in the mesopelagic carbon budget found by other studies. These are, to our best knowledge, the first high-frequency observations of export variability over the course of a full year. Our results support the deployment of bio-optical sensors on gliders to improve our understanding of the ocean carbon cycle on temporal scales from daily to annual.
Project description:To investigate the effects of H2S on the bacterial consortia on the galatheid crab, Shinkaia crosnieri, crabs of this species were cultivated in the laboratory under two different conditions, with and without hydrogen sulfide feeding. We developed a novel rearing tank system equipped with a feedback controller using a semiconductor sensor for hydrogen sulfide feeding. H2S aqueous concentration was successfully maintained between 5 to 40 µM for 80 d with the exception of brief periods of mechanical issues. According to real-time PCR analysis, the numbers of copies of partial 16S rRNA gene of an episymbiont of the crabs with H2S feeding was three orders of magnitude larger than that without feeding. By phylogenetic analysis of partial 16S rRNA gene, we detected several clones related to symbionts of deep sea organisms in Alphaproteobacteria, Gammaproteobacteria, Epsilonproteobacteria, and Flavobacteria, from a crab with H2S feeding. The symbiont-related clones were grouped into four different groups: Gammaproteobacteria in marine epibiont group I, Sulfurovum-affiliated Epsilonproteobacteria, Osedax mucofloris endosymbiont-affiliated Epsilonproteobacteria, and Flavobacteria closely related to CFB group bacterial epibiont of Rimicaris exoculata. The other phylotypes were related to Roseobacter, and some Flavobacteria, seemed to be free-living psychrophiles. Furthermore, white biofilm occurred on the surface of the rearing tank with H2S feeding. The biofilms contained various phylotypes of Gammaproteobacteria, Epsilonproteobacteria, and Flavobacteria, as determined by phylogenetic analysis. Interestingly, major clones were related to symbionts of Alviniconcha sp. type 2 and to endosymbionts of Osedax mucofloris, in Epsilonproteobacteria.
Project description:Sinking particles formed in the photic zone and moving vertically through the water column are a main mechanism for nutrient transport to the deep ocean, and a key component of the biological carbon pump. The particles appear to be processed by a microbial community substantially different from the surrounding waters. Single cell genomics and metagenomics were employed to describe the succession of dominant bacterial groups during particle processing. Sinking particles were extracted from sediment traps at Station Aloha in the North Pacific Subtropical Gyre (NPSG) during two different trap deployments conducted in July and August 2012. The microbial communities in poisoned vs. live sediment traps differed significantly from one another, consistent with prior observations by Fontanez et al. (2015). Partial genomes from these communities were sequenced from cells belonging to the genus Arcobacter (commensalists potentially associated with protists such as Radiolaria), and Vibrio campbellii (a group previously reported to be associated with crustacea). These bacteria were found in the particle-associated communities at specific depths in both trap deployments, presumably due to their specific host-associations. Partial genomes were also sequenced from cells belonging to Idiomarina and Kangiella that were enriched in live traps over a broad depth range, that represented a motile copiotroph and a putatively non-motile algicidal saprophyte, respectively. Planktonic bacterial cells most likely caught in the wake of the particles belonging to Actinomarina and the SAR11 clade were also sequenced. Our results suggest that similar groups of eukaryote-associated bacteria are consistently found on sinking particles at different times, and that particle remineralization involves specific, reproducible bacterial succession events in oligotrophic ocean waters.
Project description:In summer 2012, Arctic sea ice declined to a record minimum and, as a consequence of the melting, large amounts of aggregated ice-algae sank to the seafloor at more than 4,000 m depth. In this study, we assessed the composition, turnover and connectivity of bacterial and microbial eukaryotic communities across Arctic habitats from sea ice, algal aggregates and surface waters to the seafloor. Eukaryotic communities were dominated by diatoms, dinoflagellates and other alveolates in all samples, and showed highest richness and diversity in sea-ice habitats (?400-500 OTUs). Flavobacteriia and Gammaproteobacteria were the predominant bacterial classes across all investigated Arctic habitats. Bacterial community richness and diversity peaked in deep-sea samples (?1,700 OTUs). Algal aggregate-associated bacterial communities were mainly recruited from the sea-ice community, and were transported to the seafloor with the sinking ice algae. The algal deposits at the seafloor had a unique community structure, with some shared sequences with both the original sea-ice community (22% OTU overlap), as well as with the deep-sea sediment community (17% OTU overlap). We conclude that ice-algal aggregate export does not only affect carbon export from the surface to the seafloor, but may change microbial community composition in central Arctic habitats with potential effects for benthic ecosystem functioning in the future.
Project description:Passive sinking of particulate organic matter (POM) is the main mechanism through which the biological pump transports surface primary production to the ocean interior. However, the contribution and variability of different biological sources to vertical export is not fully understood. Here, we use DNA metabarcoding of the 18S rRNA gene and particle interceptor traps (PITs) to characterize the taxonomic composition of particles sinking out of the photic layer in the California Current Ecosystem (CCE), a productive system with high export potential. The PITs included formalin-fixed and 'live' traps to investigate eukaryotic communities involved in the export and remineralization of sinking particles. Sequences affiliated with Radiolaria dominated the eukaryotic assemblage in fixed traps (90%), with Dinophyta and Metazoa making minor contributions. The prominence of Radiolaria decreased drastically in live traps, possibly due to selective consumption by copepods, heterotrophic nanoflagellates, and phaeodarians that were heavily enriched in these traps. These patterns were consistent across the water masses surveyed extending from the coast to offshore, despite major differences in productivity and trophic structure of the epipelagic plankton community. Our findings identify Radiolaria as major actors in export fluxes in the CCE.