'Boom-and-busted' dynamics of phytoplankton-virus interactions explain the paradox of the plankton.

Rapid virus proliferation can exert a powerful control on phytoplankton host populations, playing a significant role in marine biogeochemistry and ecology. We explore how marine lytic viruses impact phytoplankton succession, affecting host and nonhost populations. Using an in silico food web we conducted simulation experiments under a range of different abiotic and biotic conditions, exploring virus-host-grazer interactions and manipulating competition, allometry, motility and cyst cycles. Virus-host and predator-prey interactions, and interactions with competitors, generate bloom dynamics with a pronounced 'boom-and-busted' dynamic (BBeD) which leads to the suppression of otherwise potentially successful phytoplankton species. The BBeD is less pronounced at low nutrient loading through distancing of phytoplankton hosts, while high sediment loading and high nonhost biomass decrease the abundance of viruses through adsorption. Larger hosts are inherently more distanced, but motility increases virus attack, while cyst cycles promote spatial and temporal distancing. Virus control of phytoplankton bloom development appears more important than virus-induced termination of those blooms. This affects plankton succession - not only the growth of species infected by the virus, but also those that compete for the same resources and are collectively subjected to common grazer control. The role of viruses in structuring plankton communities via BBeDs can thus provide an explanation for the paradox of the plankton.

Nitrous oxide and methane in a changing Arctic Ocean.

Human activities are changing the Arctic environment at an unprecedented rate resulting in rapid warming, freshening, sea ice retreat and ocean acidification of the Arctic Ocean. Trace gases such as nitrous oxide (N2O) and methane (CH4) play important roles in both the atmospheric reactivity and radiative budget of the Arctic and thus have a high potential to influence the region's climate. However, little is known about how these rapid physical and chemical changes will impact the emissions of major climate-relevant trace gases from the Arctic Ocean. The combined consequences of these stressors present a complex combination of environmental changes which might impact on trace gas production and their subsequent release to the Arctic atmosphere. Here we present our current understanding of nitrous oxide and methane cycling in the Arctic Ocean and its relevance for regional and global atmosphere and climate and offer our thoughts on how this might change over coming decades.

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.

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.

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.

MODELING THE RELEASE OF DISSOLVED ORGANIC MATTER BY PHYTOPLANKTON(1).

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.

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 large capacity for dark nitrate-assimilation in diatoms may overcome nitrate limitation of growth.

• The ability of the diatom Thalassiosira weissflogii to assimilate inorganic N in darkness is compared with that seen in flagellates. • Experiments were conducted with T. weissflogii grown in N-replete and in N-limiting cultures and the rates and capacity for ammonium and nitrate assimilation were determined. • High daily growth rates in the diatom under high-light nitrate-replete conditions are only attainable by continuing nitrate assimilation in darkness using excess C accumulated in the light when nitrate assimilation cannot match C-fixation. The ability to use ammonium in darkness is greater than for nitrate but the ratio of dark to light assimilation for each N source is similar over a wide range of cellular N : C ratios. These capabilities are in strong contrast with those in the flagellates Heterosigma carterae and Heterocapsa illdefina, which are incapable of high nitrate use in darkness. • While the possession of large capacity for dark nitrate-assimilation in diatoms may provide a mechanism that overcomes nitrate limitation of growth, the explanation for the lower capabilities exhibited by flagellates is less clear.

Modelling suggests that optimization of dark nitrogen-assimilation need not be a critical selective feature in phytoplankton.

• Alternative strategies for the dark assimilation of ammonium and nitrate into microalgae are explored using a mechanistic model of algal physiology. • The standard diatom strategy, continuation of N assimilation at high rates in darkness as long as reserve C remains, is the most advantageous. The flagellate strategy, incorporating ammonium but not nitrate at a reasonable rate in darkness, is best suited to organisms with high metabolic costs, inhabiting waters with relatively high concentrations of ammonium. The strategy of vertically migrating diatoms - accumulation of nitrate in internal pools for assimilation after return to the photic zone - is best suited to slow-growing cells in low-ammonium environments. • Differences between the strategies become less significant with increasing N-source limitation (the situation more typically encountered by flagellates and migratory species) because transport rather than post-transport assimilatory processes become most limiting. • It is suggested that optimization of dark N-assimilation is not a critical selective feature; organisms with contrasting abilities in this regard usually inhabit different water bodies and have other more fundamental phenotypic differences (e.g. motility or silicon requirements).