Deuterium in marine organic biomarkers: toward a new tool for quantifying aquatic mixotrophy.

The traditional separation between primary producers (autotrophs) and consumers (heterotrophs) at the base of the marine food web is being increasingly replaced by the paradigm that mixoplankton, planktonic protists with the nutritional ability to use both phago(hetero)trophy and photo(auto)trophy to access energy are widespread globally. Thus, many 'phytoplankton' eat, while 50% of 'protozooplankton' also perform photosynthesis. Mixotrophy may enhance primary production, biomass transfer to higher trophic levels and the efficiency of the biological pump to sequester atmospheric CO2 into the deep ocean. Although this view is gaining traction, science lacks a tool to quantify the relative contributions of autotrophy and heterotrophy in planktonic protists. This hinders our understanding of their impacts on carbon cycling within marine pelagic ecosystems. It has been shown that the hydrogen (H) isotopic signature of lipids is uniquely sensitive to heterotrophy relative to autotrophy in plants and bacteria. Here, we explored whether it is also sensitive to the trophic status in protists. The new understanding of H isotope signature of lipid biomarkers suggests it offers great potential as a novel tool for quantifying the prevalence of mixotrophy in diverse marine microorganisms and thus for investigating the implications of the 'mixoplankton' paradigm.

Reconciliation of the carbon budget in the ocean's twilight zone.

Photosynthesis in the surface ocean produces approximately 100 gigatonnes of organic carbon per year, of which 5 to 15 per cent is exported to the deep ocean. The rate at which the sinking carbon is converted into carbon dioxide by heterotrophic organisms at depth is important in controlling oceanic carbon storage. It remains uncertain, however, to what extent surface ocean carbon supply meets the demand of water-column biota; the discrepancy between known carbon sources and sinks is as much as two orders of magnitude. Here we present field measurements, respiration rate estimates and a steady-state model that allow us to balance carbon sources and sinks to within observational uncertainties at the Porcupine Abyssal Plain site in the eastern North Atlantic Ocean. We find that prokaryotes are responsible for 70 to 92 per cent of the estimated remineralization in the twilight zone (depths of 50 to 1,000 metres) despite the fact that much of the organic carbon is exported in the form of large, fast-sinking particles accessible to larger zooplankton. We suggest that this occurs because zooplankton fragment and ingest half of the fast-sinking particles, of which more than 30 per cent may be released as suspended and slowly sinking matter, stimulating the deep-ocean microbial loop. The synergy between microbes and zooplankton in the twilight zone is important to our understanding of the processes controlling the oceanic carbon sink.

Attenuation of sinking particulate organic carbon flux through the mesopelagic ocean.

The biological carbon pump, which transports particulate organic carbon (POC) from the surface to the deep ocean, plays an important role in regulating atmospheric carbon dioxide (CO2) concentrations. We know very little about geographical variability in the remineralization depth of this sinking material and less about what controls such variability. Here we present previously unpublished profiles of mesopelagic POC flux derived from neutrally buoyant sediment traps deployed in the North Atlantic, from which we calculate the remineralization length scale for each site. Combining these results with corresponding data from the North Pacific, we show that the observed variability in attenuation of vertical POC flux can largely be explained by temperature, with shallower remineralization occurring in warmer waters. This is seemingly inconsistent with conclusions drawn from earlier analyses of deep-sea sediment trap and export flux data, which suggest lowest transfer efficiency at high latitudes. However, the two patterns can be reconciled by considering relatively intense remineralization of a labile fraction of material in warm waters, followed by efficient downward transfer of the remaining refractory fraction, while in cold environments, a larger labile fraction undergoes slower remineralization that continues over a longer length scale. Based on the observed relationship, future increases in ocean temperature will likely lead to shallower remineralization of POC and hence reduced storage of CO2 by the ocean.

Observing climate change trends in ocean biogeochemistry: when and where.

Understanding the influence of anthropogenic forcing on the marine biosphere is a high priority. Climate change-driven trends need to be accurately assessed and detected in a timely manner. As part of the effort towards detection of long-term trends, a network of ocean observatories and time series stations provide high quality data for a number of key parameters, such as pH, oxygen concentration or primary production (PP). Here, we use an ensemble of global coupled climate models to assess the temporal and spatial scales over which observations of eight biogeochemically relevant variables must be made to robustly detect a long-term trend. We find that, as a global average, continuous time series are required for between 14 (pH) and 32 (PP) years to distinguish a climate change trend from natural variability. Regional differences are extensive, with low latitudes and the Arctic generally needing shorter time series (<~30 years) to detect trends than other areas. In addition, we quantify the 'footprint' of existing and planned time series stations, that is the area over which a station is representative of a broader region. Footprints are generally largest for pH and sea surface temperature, but nevertheless the existing network of observatories only represents 9-15% of the global ocean surface. Our results present a quantitative framework for assessing the adequacy of current and future ocean observing networks for detection and monitoring of climate change-driven responses in the marine ecosystem.

Southern Ocean deep-water carbon export enhanced by natural iron fertilization.

The addition of iron to high-nutrient, low-chlorophyll regions induces phytoplankton blooms that take up carbon. Carbon export from the surface layer and, in particular, the ability of the ocean and sediments to sequester carbon for many years remains, however, poorly quantified. Here we report data from the CROZEX experiment in the Southern Ocean, which was conducted to test the hypothesis that the observed north-south gradient in phytoplankton concentrations in the vicinity of the Crozet Islands is induced by natural iron fertilization that results in enhanced organic carbon flux to the deep ocean. We report annual particulate carbon fluxes out of the surface layer, at three kilometres below the ocean surface and to the ocean floor. We find that carbon fluxes from a highly productive, naturally iron-fertilized region of the sub-Antarctic Southern Ocean are two to three times larger than the carbon fluxes from an adjacent high-nutrient, low-chlorophyll area not fertilized by iron. Our findings support the hypothesis that increased iron supply to the glacial sub-Antarctic may have directly enhanced carbon export to the deep ocean. The CROZEX sequestration efficiency (the amount of carbon sequestered below the depth of winter mixing for a given iron supply) of 8,600 mol mol(-1) was 18 times greater than that of a phytoplankton bloom induced artificially by adding iron, but 77 times smaller than that of another bloom initiated, like CROZEX, by a natural supply of iron. Large losses of purposefully added iron can explain the lower efficiency of the induced bloom(6). The discrepancy between the blooms naturally supplied with iron may result in part from an underestimate of horizontal iron supply.

Links between deep-sea respiration and community dynamics.

It has been challenging to establish the mechanisms that link ecosystem functioning to environmental and resource variation, as well as community structure, composition, and compensatory dynamics. A compelling hypothesis of compensatory dynamics, known as "zero-sum" dynamics, is framed in terms of energy resource and demand units, where there is an inverse link between the number of individuals in a community and the mean individual metabolic rate. However, body size energy distributions that are nonuniform suggest a niche advantage at a particular size class, which suggests a limit to which metabolism can explain community structuring. Since 1989, the composition and structure of abyssal seafloor communities in the northeast Pacific and northeast Atlantic have varied interannually with links to climate and resource variation. Here, for the first time, class and mass-specific individual respiration rates were examined along with resource supply and time series of density and biomass data of the dominant abyssal megafauna, echinoderms. Both sites had inverse relationships between density and mean individual metabolic rate. We found fourfold variation in echinoderm respiration over interannual timescales at both sites, which were linked to shifts in species composition and structure. In the northeastern Pacific, the respiration of mobile surface deposit feeding echinoderms was positively linked to climate-driven particulate organic carbon fluxes with a temporal lag of about one year, respiring - 1-6% of the annual particulate organic carbon flux.

Microplastics in commercial marine fish species in the UK - A case study in the River Thames and the River Stour (East Anglia) estuaries.

The aim of this study was to assess the abundance of microplastics in the gastro-intestinal tracts of three commercially important fish species in the UK, to determine whether catch location, feeding habits and fish size influence the amount of microplastics within fish. Fish were collected from two rivers in the UK: the River Thames and the River Stour (East Anglia). Fish were collected from two sites in the River Thames and one site in the River Stour. Species selected were European flounder (Platichthys flesus), whiting (Merlangius merlangus), and Atlantic herring (Clupea harengus), and were chosen to represent benthic and pelagic feeding habits. Across all locations, 41.5 % of fish had ingested at least one microplastic particle (37.5 % of European flounder, 52.2 % of whiting, and 28.6 % of Atlantic herring). The average number by species was 1.98 (±3.50) microplastics/fish in European flounder, 2.46 (±3.10) microplastics/fish in whiting and 1.47 (±3.17) microplastics/fish in herring. There were no significant differences in the number or mass of microplastics in fish based on river, site, species or habitat. However, the number and mass of microplastics within benthic fish (European flounder) in the River Stour were significantly higher than in benthic fish from the River Thames. By number of microplastics, larger and heavier fish were more highly contaminated. This study enhances our understanding of microplastics in commercially important fish but highlights that fish contamination is not easily predicted by feeding habits or catch location alone. Exposure and uptake is likely to vary with changing environmental conditions. Fish size tends to be a good predictor of contamination, with larger fish generally containing more microplastics. This is the first study to directly compare concentrations of microplastics in fish from different UK rivers and the first evidence of microplastics in the River Stour.

Detection of submicron- and nanoplastics spiked in environmental fresh- and saltwater with Raman spectroscopy.

Detection of small plastic particles in environmental water samples has been a topic of increasing interest in recent years. A multitude of techniques, such as variants of Raman spectroscopy, have been employed to facilitate their analysis in such complex sample matrices. However, these studies are often conducted for a limited number of plastic types in matrices with relatively little additional materials. Thus, much remains unknown about what parameters influence the detection limits of Raman spectroscopy for more environmentally relevant samples. To address this, this study utilizes Raman spectroscopy to detect six plastic particle types; 161 and 33 nm polystyrene, < 450 nm and 36 nm poly(ethylene terephthalate), 121 nm polypropylene, and 126 nm polyethylene; spiked into artificial saltwater, artificial freshwater, North Sea, Thames River, and Elbe River water. Overall, factors such as plastic particle properties, water matrix composition, and experimental setup were shown to influence the final limits of detection.

High concentrations of plastic hidden beneath the surface of the Atlantic Ocean.

Concern over plastic pollution of the marine environment is severe. The mass-imbalance between the plastic litter supplied to and observed in the ocean currently suggests a missing sink. However, here we show that the ocean interior conceals high loads of small-sized plastic debris which can balance and even exceed the estimated plastic inputs into the ocean since 1950. The combined mass of just the three most-littered plastics (polyethylene, polypropylene, and polystyrene) of 32-651 µm size-class suspended in the top 200 m of the Atlantic Ocean is 11.6-21.1 Million Tonnes. Considering that plastics of other sizes and polymer types will be found in the deeper ocean and in the sediments, our results indicate that both inputs and stocks of ocean plastics are much higher than determined previously. It is thus critical to assess these terms across all size categories and polymer groups to determine the fate and danger of plastic contamination.

Prokaryotic niche partitioning between suspended and sinking marine particles.

Suspended particles are major organic carbon substrates for heterotrophic microorganisms in the mesopelagic ocean (100-1000 m). Nonetheless, communities associated with these particles have been overlooked compared with sinking particles, the latter generally considered as main carbon transporters to the deep ocean. This study is the first to differentiate prokaryotic communities associated with suspended and sinking particles, collected with a marine snow catcher at four environmentally distinct stations in the Scotia Sea. Amplicon sequencing of 16S rRNA gene revealed distinct prokaryotic communities associated with the two particle-types in the mixed-layer (0-100 m) and upper-mesopelagic zone (mean dissimilarity 42.5% ± 15.2%). Although common remineralising taxa were present within both particle-types, gammaproteobacterial Pseudomonadales and Vibrionales, and alphaproteobacterial Rhodobacterales were found enriched in sinking particles up to 32-fold, while Flavobacteriales (Bacteroidetes) favoured suspended particles. We propose that this niche-partitioning may be driven by organic matter properties found within both particle-types: K-strategists, specialised in the degradation of complex organic compounds, thrived on semi-labile suspended particles, while generalists r-strategists were adapted to the transient labile organic contents of sinking particles. Differences between the two particle-associated communities were more pronounced in the mesopelagic than in the surface ocean, likely resulting from exchanges between particle-pools enabled by the stronger turbulence.

Diversity, ecology and biogeochemistry of cyst-forming acantharia (radiolaria) in the oceans.

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.