Osmotrophy of dissolved organic compounds by coccolithophore populations: Fixation into particulate organic and inorganic carbon.

Coccolithophores are typically thought of as photoautotrophs, yet a few genera inhabit sub-euphotic environments with insufficient light for photosynthesis, suggesting that other carbon acquisition strategies are likely. Field experiments were performed in the northwest Atlantic (a region with potentially abundant coccolithophores). Phytoplankton populations were incubated with 14C-labeled dissolved organic carbon (DOC) compounds, acetate, mannitol, and glycerol. Coccolithophores were sorted from these populations 24 hours later using flow cytometry, and DOC uptake was measured. DOC uptake rates were as high as 10-15 moles cell-1 day-1, slow relative to photosynthesis rates (10-12 moles cell-1 day-1). Growth rates on the organic compounds were low, suggesting that osmotrophy plays more of a survival strategy in low-light situations. Assimilated DOC was found in both particulate organic carbon and calcite coccoliths (particulate inorganic carbon), suggesting that osmotrophic uptake of DOC into coccolithophore calcite is a small but notable part of the biological carbon pump and alkalinity pump paradigms.

Changing Hydrographic, Biogeochemical, and Acidification Properties in the Gulf of Maine as Measured by the Gulf of Maine North Atlantic Time Series, GNATS, Between 1998 and 2018.

The Gulf of Maine North Atlantic Time Series (GNATS) has been run since 1998, across the Gulf of Maine (GoM), between Maine and Nova Scotia. GNATS goals are to provide ocean color satellite validation and to examine change in this coastal ecosystem. We have sampled hydrographical, biological, chemical, biogeochemical, and bio-optical variables. After 2008, warm water intrusions (likely North Atlantic Slope Water [NASW]) were observed in the eastern GoM at 50-180 m depths. Shallow waters (<50 m) significantly warmed in winter, summer, and fall but cooled during spring. Surface salinity and density of the GoM also significantly increased over the 20 years. Phytoplankton standing stock and primary production showed highly-significant decreases during the period. Concentrations of phosphate increased, silicate decreased, residual nitrate [N*; nitrate-silicate] increased, and the ratio of dissolved inorganic nitrogen:phosphate decreased, suggesting increasing nitrogen limitation. Dissolved organic carbon (DOC) and its optical indices generally increased over two decades, suggesting changes to the DOC cycle. Surface seawater carbonate chemistry showed winter periods where the aragonite saturation (Ωar) dropped below 1.6 gulf-wide due to upward winter mixing of cool, corrosive water. However, associated with increased average GoM temperatures, Ωar has significantly increased. These results reinforce the hypothesis that the observed decrease in surface GoM primary production resulted from a switch from Labrador Sea Water to NASW entering the GoM. A multifactor analysis shows that decreasing GoM primary production is most significantly correlated to decreases in chlorophyll and particulate organic carbon plus increases in N* and temperature.

Osmotrophy of dissolved organic carbon by coccolithophores in darkness.

The evolutionary and ecological story of coccolithophores poses questions about their heterotrophy, surviving darkness after the end-Cretaceous asteroid impact as well as survival in the deep ocean twilight zone. Uptake of dissolved organic carbon might be an alternative nutritional strategy for supply of energy and carbon molecules. Using long-term batch culture experiments, we examined coccolithophore growth and maintenance on organic compounds in darkness. Radiolabelled experiments were performed to study the uptake kinetics. Pulse-chase experiments were used to examine the uptake into unassimilated, exchangeable pools vs assimilated, nonexchangeable pools. We found that coccolithophores were able to survive and maintain their metabolism for up to 30 d in darkness, accomplishing about one cell division. The concentration dependence for uptake was similar to the concentration dependence for growth in Cruciplacolithus neohelis, suggesting that it was taking up carbon compounds and immediately incorporating them into biomass. We recorded net incorporation of radioactivity into the particulate inorganic fraction. We conclude that osmotrophy provides nutritional flexibility and supports long-term survival in light intensities well below threshold for photosynthesis. The incorporation of dissolved organic matter into particulate inorganic carbon, raises fundamental questions about the role of the alkalinity pump and the alkalinity balance in the sea.

Coccolith dissolution within copepod guts affects fecal pellet density and sinking rate.

The most common biomineral produced in the contemporary ocean is calcium carbonate, including the polymorph calcite produced by coccolithophores. The surface waters of the ocean are supersaturated with respect to calcium carbonate. As a result, particulate inorganic carbon (PIC), such as calcite coccoliths, is not expected thermodynamically to dissolve in waters above the lysocline (~4500-6000 m). However, observations indicate that up to 60-80% of calcium carbonate is lost in the upper 500-1000 m of the ocean. This is hypothesized to occur in microenvironments with reduced saturation states, such as zooplankton guts. Using a new application of the highly precise 14C microdiffusion technique, we show that following a period of starvation, up to 38% of ingested calcite dissolves in copepod guts. After continued feeding, our data show the gut becomes increasingly buffered, which limits further dissolution; this has been termed the Tums hypothesis (after the drugstore remedy for stomach acid). As less calcite dissolves in the gut and is instead egested in fecal pellets, the fecal pellet sinking rates double, with corresponding increases in pellet density. Our results empirically demonstrate that zooplankton guts can facilitate calcite dissolution above the chemical lysocline, and that carbon export through fecal pellet production is variable, based on the feeding history of the copepod.

Vertical Distributions of Coccolithophores, PIC, POC, Biogenic Silica, and Chlorophyll a Throughout the Global Ocean.

Coccolithophores are a critical component of global biogeochemistry, export fluxes, and seawater optical properties. We derive globally significant relationships to estimate integrated coccolithophore and coccolith concentrations as well as integrated concentrations of particulate inorganic carbon (PIC) from their respective surface concentration. We also examine surface versus integral relationships for other biogeochemical variables contributed by all phytoplankton (e.g., chlorophyll a and particulate organic carbon) or diatoms (biogenic silica). Integrals are calculated using both 100 m integrals and euphotic zone integrals (depth of 1% surface photosynthetically available radiation). Surface concentrations are parameterized in either volumetric units (e.g., m-3) or values integrated over the top optical depth. Various relationships between surface concentrations and integrated values demonstrate that when surface concentrations are above a specific threshold, the vertical distribution of the property is biased to the surface layer, and when surface concentrations are below a specific threshold, the vertical distributions of the properties are biased to subsurface maxima. Results also show a highly predictable decrease in explained-variance as vertical distributions become more vertically heterogeneous. These relationships have fundamental utility for extrapolating surface ocean color remote sensing measurements to 100 m depth or to the base of the euphotic zone, well beyond the depths of detection for passive ocean color remote sensors. Greatest integrated concentrations of PIC, coccoliths, and coccolithophores are found when there is moderate stratification at the base of the euphotic zone.