Darren R. Clark

The significance of nitrification for oceanic new production

The flux of organic material sinking to depth is a major control on the inventory of carbon in the ocean. To first order, the oceanic system is at equilibrium such that what goes down must come up. Because the export flux is difficult to measure directly, it is routinely estimated indirectly by quantifying the amount of phytoplankton growth, or primary production, fuelled by the upward flux of nitrate. To do so it is necessary to take into account other sources of biologically available nitrogen. However, the generation of nitrate by nitrification in surface waters has only recently received attention. Here we perform the first synthesis of open-ocean measurements of the specific rate of surface nitrification and use these to configure a global biogeochemical model to quantify the global role of nitrification. We show that for much of the world ocean a substantial fraction of the nitrate taken up is generated through recent nitrification near the surface. At the global scale, nitrification accounts for about half of the nitrate consumed by growing phytoplankton. A consequence is that many previous attempts to quantify marine carbon export, particularly those based on inappropriate use of the f-ratio (a measure of the efficiency of the ‘biological pump’), are significant overestimates.

The relationship between the dissolved inorganic carbon concentration and growth rate in marine phytoplankton

A range of marine phytoplankton was grown in closed systems in order to investigate the kinetics of dissolved inorganic carbon (DIC) use and the influence of the nitrogen source under conditions of constant pH. The kinetics of DIC use could be described by a rectangular hyperbolic curve, yielding estimations of KG(DIG) (the half saturation constant for carbon–specific growth, i.e. Cμ) and μmax (the theoretical maximum Cμ). All species attained a KG(DIC) within the range of 30–750μM DIC. For most species, NH+4 use enabled growth with a lower KG(DIC) and/or, for two species, an increase in μmax. At DIC concentrations of > 1.6 mM, Cμ was > 90% saturated for all species relative to the rate at the natural seawater DIC concentration of 2.0 mM. The results suggest that neither the rate nor the extent of primary productivity will be significantly limited by the DIC in the quasi–steady–state conditions associated with oligotrophic oceans. The method needs to be applied in the conditions associated with dynamic coastal (eutrophic) systems for clarification of a potential DIC rate limitation where cells may grow to higher densities and under variable pH and nitrogen supply.

Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession

Human activity causes ocean acidification (OA) though the dissolution of anthropogenically generated CO2 into seawater, and eutrophication through the addition of inorganic nutrients. Eutrophication increases the phytoplankton biomass that can be supported during a bloom, and the resultant uptake of dissolved inorganic carbon during photosynthesis increases water-column pH (bloom-induced basification). This increased pH can adversely affect plankton growth. With OA, basification commences at a lower pH. Using experimental analyses of the growth of three contrasting phytoplankton under different pH scenarios, coupled with mathematical models describing growth and death as functions of pH and nutrient status, we show how different conditions of pH modify the scope for competitive interactions between phytoplankton species. We then use the models previously configured against experimental data to explore how the commencement of bloom-induced basification at lower pH with OA, and operating against a background of changing patterns in nutrient loads, may modify phytoplankton growth and competition. We conclude that OA and changed nutrient supply into shelf seas with eutrophication or de-eutrophication (the latter owing to pollution control) has clear scope to alter phytoplankton succession, thus affecting future trophic dynamics and impacting both biogeochemical cycling and fisheries.

MODELING THE RELEASE OF DISSOLVED ORGANIC MATTER BY PHYTOPLANKTON1

Three models describing dissolved organic matter (DOM) flux and phytoplankton death, each of different levels of complexity, were constructed and tested against experimental data for a cyanobacterium, a chlorophyte, two diatoms, two dinoflagellates, and two prymnesiophytes. The simplest model described only bulk carbon (C) and nitrogen (N) forms of DOM (DOMC and DOMN) and employed a fixed relationship between phytoplankton nutrient status and DOM release and death rate. The most complex model described fractions of DOM as low molecular weight dissolved organic carbon (DOC; saccharides, low molecular weight carbohydrates [DOCs]), low molecular weight nitrogenous material (comprising C and N as DOC associated with low molecular weight compounds containing amino acids and/or nucleic acids [DOCa] and N associated with DOCa [DONa], which included dissolved free amino acids [DFAA]), and more complex materials (DOC associated with high molecular weight compounds typically requiring extracellular degradation prior to uptake or use by microbes [DOCx] and N associated with DOCx [DONx]). It also employed descriptions of DOM flux and cell death related to nutrient status and growth rates. In all instances, material lysed from dead cells contributed to the DOM pool. All three models captured the gross dynamics of the primary data (dissolved inorganic C [DIC], dissolved inorganic N [DIN], particulate organic carbon [POC], particulate organic N [PON], DOC, dissolved organic N [DON]), but there was little or no improvement of the fit with increasing model complexity. However, the simplest models tended to employ excessively high growth rates to compensate for high fixed death rates. While the proportion of newly fixed C being liberated as DOMC (DOCs plus DOCa) increased as nutrient status declined, the actual rate of release typically did not do so and often declined. The most complex model gave predictions for changes in released saccharides and DFAA in keeping with expectations. The major obstacle to future progress is the lack of suitable, mass balanced data sets for further model testing.

Variation in elemental stoichiometry of the marine diatom Thalassiosira weissflogii (Bacillariophyceae) in response to combined nutrient stress and changes in carbonate chemistry.

The combined consequences of the multi‐stressors of pH and nutrient availability upon the growth of a marine diatom were investigated. Thalassiosira weissflogii was grown in N‐ or P‐limited batch culture in sealed systems, with pH commencing at 8.2 (“extant” conditions) or 7.6 (“ocean acidification” [OA] conditions), and then pH was allowed to either drift with growth, or was held fixed. Results indicated that within the pH range tested, the stability of environmental pH rather than its value (i.e., OA vs. extant) fundamentally influenced biomass accumul‐ation and C:N:P stoichiometry. Despite large changes in total alkalinity in the fixed pH systems, final biomass production was consistently greater in these systems than that in drifting pH systems. In drift systems, pH increased to exceed pH 9.5, a level of alkalinity that was inhibitory to growth. No statis‐tically significant differences between pH treatments were measured for N:C, P:C or N:P ratios during nutrient‐replete growth, although the diatom expre‐ssed greater plasticity in P:C and N:P ratios than in N:C during this growth phase. During nutrient‐deplete conditions, the capacity for uncoupled carbon fixa‐tion at fixed pH was considerably greater than that measured in drift pH systems, leading to strong contrasts in C:N:P stoichiometry between these treatments. Whether environmental pH was stable or drifted directly influenced the extent of physiological stress. In contrast, few distinctions could be drawn between “extant” versus “OA” conditions for cell physiology.

Biological or microbial carbon pump? The role of phytoplankton stoichiometry in ocean carbon sequestration

Once fixed by photosynthesis carbon becomes part of the marine food web. The fate of this carbon has two possible outcomes: it may be respired and released back to the ocean and potentially to the atmosphere as CO2 or retained in the ocean interior and/or marine sediments for extended time scales. The most important biologically mediated processes responsible for long term carbon storage in the ocean are the biological carbon pump (BCP) and the microbial carbon pump (MCP). While acting simultaneously in the ocean, the balance between these two mechanisms is thought to vary depending on the trophic state of the environment. Using previously published formulations, we propose a modelling framework to simulate variability in the MCP: BCP ratio as a function of external nutrients. Our results suggest that the role of the MCP might become more significant under future climate change conditions where increased stratification enhances the oligotrophic nature of the surface ocean. Based on these model results, we propose a conceptual framework in which the internal stoichiometry of phytoplankton, modulating both grazing pressure and DOM production (via phytoplankton exudation), plays a crucial role in regulating the MCP: BCP ratio.

The role of coccolithophore calcification in bioengineering their environment.

Coccolithophorids are enigmatic plankton that produce calcium carbonate coccoliths, which over geological time have buried atmospheric CO2 into limestone, changing both the atmosphere and geology of the Earth. However, the role of coccoliths for the proliferation of these organisms remains unclear; suggestions include roles in anti-predation, enhanced photosynthesis and sun-screening. Here we test the hypothesis that calcification stabilizes the pH of the seawater proximate to the organisms, providing a level of acidification countering the detrimental basification that occurs during net photosynthesis. Such bioengineering provides a more stable pH environment for growth and fits the empirical evidence for changes in rates of calcification under different environmental conditions. Under this scenario, simulations suggest that the optimal production ratio of inorganic to organic particulate C (PIC : POCprod) will be lower (by approx. 20%) with ocean acidification and that overproduction of coccoliths in a future acidified ocean, where pH buffering is weaker, presents a risk to calcifying cells.

A substantial fraction of phytoplankton-derived DON is resistant to degradation by a metabolically versatile, widely distributed marine bacterium

The capacity of bacteria for degrading dissolved organic nitrogen (DON) and remineralising ammonium is of importance for marine ecosystems, as nitrogen availability frequently limits productivity. Here, we assess the capacity of a widely distributed and metabolically versatile marine bacterium to degrade phytoplankton-derived dissolved organic carbon (DOC) and nitrogen. To achieve this, we lysed exponentially growing diatoms and used the derived dissolved organic matter (DOM) to support an axenic culture of Alteromonas sp.. Bacterial biomass (as particulate carbon and nitrogen) was monitored for 70 days while growth dynamics (cell count), DOM (DOC, DON) and dissolved nutrient concentrations were monitored for up to 208 days. Bacterial biomass increased rapidly within the first 7 days prior to a period of growth/death cycles potentially linked to rapid nutrient recycling. We found that ≈75% of the initial DOC and ≈35% of the initial DON were consumed by bacteria within 40 and 4 days respectively, leaving a significant fraction of DOM resilient to degradation by this bacterial species. The different rates and extents to which DOC and DON were accessed resulted in changes in DOM stoichiometry and the iterative relationship between DOM quality and bacterial growth over time influenced bacterial cell C:N molar ratio. C:N values increased to 10 during the growth phase before decreasing to values of ≈5, indicating a change from relative N-limitation/C-sufficiency to relative C-limitation/N-sufficiency. Consequently, despite its reported metabolic versatility, we demonstrate that Alteromonas sp. was unable to access all phytoplankton derived DOM and that a bacterial community is likely to be required. By making the relatively simple assumption that an experimentally derived fraction of DOM remains resilient to bacterial degradation, these experimental results were corroborated by numerical simulations using a previously published model describing the interaction between DOM and bacteria in marine systems, thus supporting our hypothesis.