Enhanced silica export in a future ocean triggers global diatom decline.

Diatoms account for up to 40% of marine primary production1,2 and require silicic acid to grow and build their opal shell3. On the physiological and ecological level, diatoms are thought to be resistant to, or even benefit from, ocean acidification4-6. Yet, global-scale responses and implications for biogeochemical cycles in the future ocean remain largely unknown. Here we conducted five in situ mesocosm experiments with natural plankton communities in different biomes and find that ocean acidification increases the elemental ratio of silicon (Si) to nitrogen (N) of sinking biogenic matter by 17 ± 6 per cent under [Formula: see text] conditions projected for the year 2100. This shift in Si:N seems to be caused by slower chemical dissolution of silica at decreasing seawater pH. We test this finding with global sediment trap data, which confirm a widespread influence of pH on Si:N in the oceanic water column. Earth system model simulations show that a future pH-driven decrease in silica dissolution of sinking material reduces the availability of silicic acid in the surface ocean, triggering a global decline of diatoms by 13-26 per cent due to ocean acidification by the year 2200. This outcome contrasts sharply with the conclusions of previous experimental studies, thereby illustrating how our current understanding of biological impacts of ocean change can be considerably altered at the global scale through unexpected feedback mechanisms in the Earth system.

The appendicularian Oikopleura dioica can enhance carbon export in a high CO2 ocean.

Gelatinous zooplankton are increasingly recognized to play a key role in the ocean's biological carbon pump. Appendicularians, a class of pelagic tunicates, are among the most abundant gelatinous plankton in the ocean, but it is an open question how their contribution to carbon export might change in the future. Here, we conducted an experiment with large volume in situ mesocosms (~55-60 m3 and 21 m depth) to investigate how ocean acidification (OA) extreme events affect food web structure and carbon export in a natural plankton community, particularly focusing on the keystone species Oikopleura dioica, a globally abundant appendicularian. We found a profound influence of O. dioica on vertical carbon fluxes, particularly during a short but intense bloom period in the high CO2 treatment, during which carbon export was 42%-64% higher than under ambient conditions. This elevated flux was mostly driven by an almost twofold increase in O. dioica biomass under high CO2 . This rapid population increase was linked to enhanced fecundity (+20%) that likely resulted from physiological benefits of low pH conditions. The resulting competitive advantage of O. dioica resulted in enhanced grazing on phytoplankton and transfer of this consumed biomass into sinking particles. Using a simple carbon flux model for O. dioica, we estimate that high CO2 doubled the carbon flux of discarded mucous houses and fecal pellets, accounting for up to 39% of total carbon export from the ecosystem during the bloom. Considering the wide geographic distribution of O. dioica, our findings suggest that appendicularians may become an increasingly important vector of carbon export with ongoing OA.

Exploring biogeochemical and ecological redundancy in phytoplankton communities in the global ocean.

Climate-change-induced alterations of oceanic conditions will lead to the ecological niches of some marine phytoplankton species disappearing, at least regionally. How will such losses affect the ecosystem and the coupled biogeochemical cycles? Here, we couch this question in terms of ecological redundancy (will other species be able to fill the ecological roles of the extinct species) and biogeochemical redundancy (can other species replace their biogeochemical roles). Prior laboratory and field studies point to a spectrum in the degree of redundancy. We use a global three-dimensional computer model with diverse planktonic communities to explore these questions further. The model includes 35 phytoplankton types that differ in size, biogeochemical function and trophic strategy. We run two series of experiments in which single phytoplankton types are either partially or fully eliminated. The niches of the targeted types were not completely reoccupied, often with a reduction in the transfer of matter from autotrophs to heterotrophs. Primary production was often decreased, but sometimes increased due to reduction in grazing pressure. Complex trophic interactions (such as a decrease in the stocks of a predator's grazer) led to unexpected reshuffling of the community structure. Alterations in resource utilization may cause impacts beyond the regions where the type went extinct. Our results suggest a lack of redundancy, especially in the 'knock on' effects on higher trophic levels. Redundancy appeared lowest for types on the edges of trait space (e.g. smallest) or with unique competitive strategies. Though highly idealized, our modelling findings suggest that the results from laboratory or field studies often do not adequately capture the ramifications of functional redundancy. The modelled, often counterintuitive, responses-via complex food web interactions and bottom-up versus top-down controls-indicate that changes in planktonic community will be key determinants of future ocean global change ecology and biogeochemistry.

Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change-A review.

Marine life is controlled by multiple physical and chemical drivers and by diverse ecological processes. Many of these oceanic properties are being altered by climate change and other anthropogenic pressures. Hence, identifying the influences of multifaceted ocean change, from local to global scales, is a complex task. To guide policy-making and make projections of the future of the marine biosphere, it is essential to understand biological responses at physiological, evolutionary and ecological levels. Here, we contrast and compare different approaches to multiple driver experiments that aim to elucidate biological responses to a complex matrix of ocean global change. We present the benefits and the challenges of each approach with a focus on marine research, and guidelines to navigate through these different categories to help identify strategies that might best address research questions in fundamental physiology, experimental evolutionary biology and community ecology. Our review reveals that the field of multiple driver research is being pulled in complementary directions: the need for reductionist approaches to obtain process-oriented, mechanistic understanding and a requirement to quantify responses to projected future scenarios of ocean change. We conclude the review with recommendations on how best to align different experimental approaches to contribute fundamental information needed for science-based policy formulation.

Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification.

Coccolithophores are unicellular marine algae that produce biogenic calcite scales and substantially contribute to marine primary production and carbon export to the deep ocean. Ongoing ocean acidification particularly impairs calcifying organisms, mostly resulting in decreased growth and calcification. Recent studies revealed that the immediate physiological response in the coccolithophore Emiliania huxleyi to ocean acidification may be partially compensated by evolutionary adaptation, yet the underlying molecular mechanisms are currently unknown. Here, we report on the expression levels of 10 candidate genes putatively relevant to pH regulation, carbon transport, calcification and photosynthesis in E. huxleyi populations short-term exposed to ocean acidification conditions after acclimation (physiological response) and after 500 generations of high CO2 adaptation (adaptive response). The physiological response revealed downregulation of candidate genes, well reflecting the concomitant decrease of growth and calcification. In the adaptive response, putative pH regulation and carbon transport genes were up-regulated, matching partial restoration of growth and calcification in high CO2-adapted populations. Adaptation to ocean acidification in E. huxleyi likely involved improved cellular pH regulation, presumably indirectly affecting calcification. Adaptive evolution may thus have the potential to partially restore cellular pH regulatory capacity and thereby mitigate adverse effects of ocean acidification.

Diatom-mediated food web functioning under ocean artificial upwelling.

Enhancing ocean productivity by artificial upwelling is evaluated as a nature-based solution for food security and climate change mitigation. Fish production is intended through diatom-based plankton food webs as these are assumed to be short and efficient. However, our findings from mesocosm experiments on artificial upwelling in the oligotrophic ocean disagree with this classical food web model. Here, diatoms did not reduce trophic length and instead impaired the transfer of primary production to crustacean grazers and small pelagic fish. The diatom-driven decrease in trophic efficiency was likely mediated by changes in nutritional value for the copepod grazers. Whilst diatoms benefitted the availability of essential fatty acids, they also caused unfavorable elemental compositions via high carbon-to-nitrogen ratios (i.e. low protein content) to which the grazers were unable to adapt. This nutritional imbalance for grazers was most pronounced in systems optimized for CO2 uptake through carbon-to-nitrogen ratios well beyond Redfield. A simultaneous enhancement of fisheries production and carbon sequestration via artificial upwelling may thus be difficult to achieve given their opposing stoichiometric constraints. Our study suggest that food quality can be more critical than quantity to maximize food web productivity during shorter-term fertilization of the oligotrophic ocean.

Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi.

Coccolithophores are important calcifying phytoplankton predicted to be impacted by changes in ocean carbonate chemistry caused by the absorption of anthropogenic CO2 . However, it is difficult to disentangle the effects of the simultaneously changing carbonate system parameters (CO2 , bicarbonate, carbonate and protons) on the physiological responses to elevated CO2 . Here, we adopted a multifactorial approach at constant pH or CO2 whilst varying dissolved inorganic carbon (DIC) to determine physiological and transcriptional responses to individual carbonate system parameters. We show that Emiliania huxleyi is sensitive to low CO2 (growth and photosynthesis) and low bicarbonate (calcification) as well as low pH beyond a limited tolerance range, but is much less sensitive to elevated CO2 and bicarbonate. Multiple up-regulated genes at low DIC bear the hallmarks of a carbon-concentrating mechanism (CCM) that is responsive to CO2 and bicarbonate but not to pH. Emiliania huxleyi appears to have evolved mechanisms to respond to limiting rather than elevated CO2 . Calcification does not function as a CCM, but is inhibited at low DIC to allow the redistribution of DIC from calcification to photosynthesis. The presented data provides a significant step in understanding how E. huxleyi will respond to changing carbonate chemistry at a cellular level.

Impact of green and blue-green light on the growth, pigment concentration, and fatty acid unsaturation in the microalga Monoraphidium braunii.

The spectral composition of light is an important factor for the metabolism of photosynthetic organisms. Several blue light-regulated metabolic processes have already been identified in the industrially relevant microalga Monoraphidium braunii. However, little is known about the spectral impact on this species' growth, fatty acid (FA), and pigment composition. In this study, M. braunii was cultivated under different light spectra (white light: 400-700 nm, blue light: 400-550 nm, green light: 450-600 nm, and red light: 580-700 nm) at 25°C for 96 h. The growth was monitored daily. Additionally, the FA composition, and pigment concentration was analyzed after 96 h. The highest biomass production was observed upon white light and red light irradiation. However, green light also led to comparably high biomass production, fueling the scientific debate about the contribution of weakly absorbed light wavelengths to microalgal biomass production. All light spectra (white, blue, and green) that comprised blue-green light (450-550 nm) led to a higher degree of FA unsaturation and a greater concentration of all identified pigments than red light. These results further contribute to the growing understanding that blue-green light is an essential trigger for maximized pigment concentration and FA unsaturation in green microalgae.

Respiration rate scales inversely with sinking speed of settling marine aggregates.

Sinking marine aggregates have been studied for a long time to understand their role in carbon sequestration. Traditionally, sinking speed and respiration rates have been treated as independent variables, but two recent papers suggest that there is a connection albeit in contrasting directions. Here we collected recently formed (<2 days old) aggregates from sediment traps mounted underneath mesocosms during two different experiments. The mesocosms were moored off Gran Canaria, Spain (~ 27.9 N; 15.4 E) in a coastal, sub-tropical and oligotrophic ecosystem. We determined the respiration rates of organisms (mainly heterotrophic prokaryotes) attached to aggregates sinking at different velocities. The average respiration rate of fast sinking aggregates (>100 m d-1) was 0.12 d-1 ± 0.08 d-1 (SD). Slower sinking aggregates (<50 m d-1) had on average higher (p <0.001) and more variable respiration rates (average 0.31 d-1 ± 0.16 d-1, SD). There was evidence that slower sinking aggregates had higher porosity than fast sinking aggregates, and we hypothesize that higher porosity increase the settlement area for bacteria and the respiration rate. These findings provide insights into the efficiency of the biological carbon pump and help resolve the apparent discrepancy in the recent studies of the correlation between respiration and sinking speed.

Sensitivities of marine carbon fluxes to ocean change.

Throughout Earth's history, the oceans have played a dominant role in the climate system through the storage and transport of heat and the exchange of water and climate-relevant gases with the atmosphere. The ocean's heat capacity is approximately 1,000 times larger than that of the atmosphere, its content of reactive carbon more than 60 times larger. Through a variety of physical, chemical, and biological processes, the ocean acts as a driver of climate variability on time scales ranging from seasonal to interannual to decadal to glacial-interglacial. The same processes will also be involved in future responses of the ocean to global change. Here we assess the responses of the seawater carbonate system and of the ocean's physical and biological carbon pumps to (i) ocean warming and the associated changes in vertical mixing and overturning circulation, and (ii) ocean acidification and carbonation. Our analysis underscores that many of these responses have the potential for significant feedback to the climate system. Because several of the underlying processes are interlinked and nonlinear, the sign and magnitude of the ocean's carbon cycle feedback to climate change is yet unknown. Understanding these processes and their sensitivities to global change will be crucial to our ability to project future climate change.

Changes in biogenic carbon flow in response to sea surface warming.

The pelagic ocean harbors one of the largest ecosystems on Earth. It is responsible for approximately half of global primary production, sustains worldwide fisheries, and plays an important role in the global carbon cycle. Ocean warming caused by anthropogenic climate change is already starting to impact the marine biota, with possible consequences for ocean productivity and ecosystem services. Because temperature sensitivities of marine autotrophic and heterotrophic processes differ greatly, ocean warming is expected to cause major shifts in the flow of carbon and energy through the pelagic system. Attempts to integrate such biological responses into marine ecosystem and biogeochemical models suffer from a lack of empirical data. Here, we show, using an indoor-mesocosm approach, that rising temperature accelerates respiratory consumption of organic carbon relative to autotrophic production in a natural plankton community. Increasing temperature by 2-6 degrees C hence decreased the biological drawdown of dissolved inorganic carbon in the surface layer by up to 31%. Moreover, warming shifted the partitioning between particulate and dissolved organic carbon toward an enhanced accumulation of dissolved compounds. In line with these findings, the loss of organic carbon through sinking was significantly reduced at elevated temperatures. The observed changes in biogenic carbon flow have the potential to reduce the transfer of primary produced organic matter to higher trophic levels, weaken the ocean's biological carbon pump, and hence provide a positive feedback to rising atmospheric CO(2).

Blue-green light is required for a maximized fatty acid unsaturation and pigment concentration in the microalga Acutodesmus obliquus.

Blue-green light is known to maximize the degree of fatty acid (FA) unsaturation in microalgae. However, knowledge on the particular waveband responsible for this stimulation of FA desaturation and its impact on the pigment composition in microalgae remains limited. In this study, Acutodesmus obliquus was cultivated for 96 h at 15°C with different light spectra (380-700 nm, 470-700 nm, 520-700 nm, 600-700 nm, and dark controls). Growth was monitored daily, and qualitative characterization of the microalgal FA composition was achieved via gas chromatography coupled with electron impact ionization mass spectrometry (GC-EI/MS). Additionally, a quantitative analysis of microalgal pigments was performed using high-performance liquid chromatography with diode array detection (HPLC-DAD). Spectra that included wavelengths between 470 and 520 nm led to a significantly higher percentage of the polyunsaturated fatty acids (PUFA) 18:3 and 16:4, compared to all other light conditions. However, no significant differences between the red light cultivations and the heterotrophic dark controls were observed for the FA 18:3 and 16:4. These results indicate, that exclusively the blue-green light waveband between 470 and 520 nm is responsible for a maximized FA unsaturation in A. obliquus. Furthermore, the growth and production of pigments were impaired if blue-green light (380-520 nm) was absent in the light spectrum. This knowledge can contribute to achieving a suitable microalgal pigment and FA composition for industrial purposes and must be considered in spectrally selective microalgae cultivation systems.

Differences in adaptation to light and temperature extremes of Chlorella sorokiniana strains isolated from a wastewater lagoon.

Presently, two Chlorella sorokiniana strains sampled during summer (CS-S) and winter (CS-W) from a maturation pond and isolated by dominance were studied on their behavior on temperature and light extremes in batch experiments. Although both strains showed no differences in their tolerance of temperatures up to 45 °C, the growth rates, pigment contents and fatty acid compositions in response to PAR at 700 and 1,500 µmol m-2sec-1 differed. CS-W was less affected by photoinhibition and maintained constantly high growth rates. High radiation resulted in both strains in an equivalent decrease of chlorophyll a and accessory pigments indicating that the latter did not function as a light filter. PUFAS (18:3 and 16:3) increased in CS-W at high radiation by > 60% and decreased in CS-S by 8 %. Results indicate that CS-W is highly favorable for mass cultivation particularly in outdoors, in which diurnal variations of solar radiation occur.

Ocean acidification induces distinct metabolic responses in subtropical zooplankton under oligotrophic conditions and after simulated upwelling.

Ocean acidification (OA) is one of the most critical anthropogenic threats to marine ecosystems. While significant ecological responses of plankton communities to OA have been revealed mainly by small-scale laboratory approaches, the interactive effect of OA-related changes on zooplankton metabolism and their biogeochemical implications in the natural environment still remains less well understood. Here, we explore the responses of zooplankton respiration and ammonium excretion, two key processes in the nutrient cycling, to high pCO2 levels in a 9-week in situ mesocosm experiment conducted during the autumn oligotrophic season in the subtropical northeast Atlantic. By simulating an upwelling event halfway through the study, we further evaluated the combined effects of OA and nutrient availability on the physiology of micro-and mesozooplankton. OA conditions generally resulted in a reduction in the biomass-specific metabolic and enzymatic rates, particularly in the mesozooplankton community. The situation reversed after the nutrient-rich deep-water addition, which initially promoted a diatom bloom and increased heterotrophic activities in all mesocosms. Under high pCO2 conditions (>800 µatm), however, the nutrient fertilization triggered the proliferation of the harmful alga Vicicitus globosus, with important consequences for the metabolic performance of the two zooplankton size classes. Here, the zooplankton contribution to the remineralization of organic matter and nitrogen regeneration dropped by 30% and 24%, respectively, during the oligotrophic period, and by 40% and 70% during simulated upwelling. Overall, our results indicate a potential reduction in the biogeochemical role of zooplankton under future ocean conditions, with more evident effects on the large mesozooplankton and during high productivity events.

Expression of biomineralization-related ion transport genes in Emiliania huxleyi.

Biomineralization in the marine phytoplankton Emiliania huxleyi is a stringently controlled intracellular process. The molecular basis of coccolith production is still relatively unknown although its importance in global biogeochemical cycles and varying sensitivity to increased pCO2 levels has been well documented. This study looks into the role of several candidate Ca²âº, H⁺ and inorganic carbon transport genes in E. huxleyi, using quantitative reverse transcriptase PCR. Differential gene expression analysis was investigated in two isogenic pairs of calcifying and non-calcifying strains of E. huxleyi and cultures grown at various Ca²âº concentrations to alter calcite production. We show that calcification correlated to the consistent upregulation of a putative HCO3⁻ transporter belonging to the solute carrier 4 (SLC4) family, a Ca²âº/H⁺ exchanger belonging to the CAX family of exchangers and a vacuolar H⁺-ATPase. We also show that the coccolith-associated protein, GPA is downregulated in calcifying cells. The data provide strong evidence that these genes play key roles in E. huxleyi biomineralization. Based on the gene expression data and the current literature a working model for biomineralization-related ion transport in coccolithophores is presented.

Polysaccharide aggregation as a potential sink of marine dissolved organic carbon.

The formation and sinking of biogenic particles mediate vertical mass fluxes and drive elemental cycling in the ocean. Whereas marine sciences have focused primarily on particle production by phytoplankton growth, particle formation by the assembly of organic macromolecules has almost been neglected. Here we show, by means of a combined experimental and modelling study, that the formation of polysaccharide particles is an important pathway to convert dissolved into particulate organic carbon during phytoplankton blooms, and can be described in terms of aggregation kinetics. Our findings suggest that aggregation processes in the ocean cascade from the molecular scale up to the size of fast-settling particles, and give new insights into the cycling and export of biogeochemical key elements such as carbon, iron and thorium.

Oxidative stress and antioxidant defence responses in two marine copepods in a high CO2 experiment.

We collected samples for oxidative stress and antioxidants in a high CO2 mesocosm experiment for two weeks, focussing on two common crustacean copepods Calanus finmarchicus and Temora longicornis. The samples were collected during a field experiment campaign studying responses of plankton communities to future ocean acidification (OA), off the Norwegian coast south of Bergen. The main results showed that there were species-specific differences between Temora and Calanus, especially in antioxidant defences (glutathione system) and oxidative stress (lipid peroxidation and reduced:oxidised glutathione ratio). Regular monitoring of chlorophyll a and jellyfish abundances taking place during the field campaign revealed that both chl a and predators may have affected the eco-physiological response. Antioxidant and oxidative stress levels are known to respond sensitively to both the food quality and quantity and the predator pressure, apart from environmental (i.e., abiotic) changes. Calanus was more robust towards OA, perhaps due to its high tolerance to a wide range of vertical physical-chemical conditions. Both top-down and bottom-up factors seem to play a role for the outcome of copepod responses to future ocean acidification.

Ocean acidification increases domoic acid contents during a spring to summer succession of coastal phytoplankton.

Enrichment of the oceans with CO2 may be beneficial for some marine phytoplankton, including harmful algae. Numerous laboratory experiments provided valuable insights into the effects of elevated pCO2 on the growth and physiology of harmful algal species, including the production of phycotoxins. Experiments close to natural conditions are the next step to improve predictions, as they consider the complex interplay between biotic and abiotic factors that can confound the direct effects of ocean acidification. We therefore investigated the effect of ocean acidification on the occurrence and abundance of phycotoxins in bulk plankton samples during a long-term mesocosm experiment in the Gullmar Fjord, Sweden, an area frequently experiencing harmful algal blooms. During the experimental period, a total of seven phycotoxin-producing harmful algal genera were identified in the fjord, and in accordance, six toxin classes were detected. However, within the mesocosms, only domoic acid and the corresponding producer Pseudo-nitzschia spp. was observed. Despite high variation within treatments, significantly higher particulate domoic acid contents were measured in the mesocosms with elevated pCO2. Higher particulate domoic acid contents were additionally associated with macronutrient limitation. The risks associated with potentially higher phycotoxin levels in the future ocean warrants attention and should be considered in prospective monitoring strategies for coastal marine waters.