Description: The subtropical oceans are home to the largest phytoplankton biome on the planet. Yet, little is known about potential impacts of ocean acidification (OA) on phytoplankton community composition in the vast oligotrophic ecosystems of the subtropical gyres. To address this question, we conducted an experiment with 9 in situ mesocosms (~35 m3) off the coast of Gran Canaria in the eastern subtropical North Atlantic over a period of 9 weeks. By establishing a gradient of pCO2 ranging from ~350 to 1025 µatm, we simulated carbonate chemistry conditions as projected until the end of the 21st century. Furthermore, we injected nutrient-rich deep water into the mesocosms halfway through the experiment to simulate a natural upwelling event, which regularly leads to patchy nutrient fertilization in the study region. The temporal developments of major taxonomic groups of phytoplankton were analyzed by flow cytometry, pigment composition and microscopy. We observed distinct shifts in phytoplankton community structure in response to high CO2, with markedly different patterns depending on nutrient status of the system. Phytoplankton biomass during the oligotrophic phase was dominated by picocyanobacteria (Synechococcus), which constituted 60-80% of biomass and displayed significantly higher cell abundances at elevated pCO2. The addition of deep water triggered a substantial bloom of large, chain-forming diatoms (mainly Guinardia striata and Leptocylindrus danicus) that dominated the phytoplankton community during the bloom phase (70-80% of biomass) and until the end of the experiment. A CO2 effect on bulk diatom biomass became apparent only in the highest CO2 treatments (〉800 µatm), displaying elevated concentrations especially in the stationary phase after nutrient depletion. Notably, these responses were tightly linked to distinct interspecific shifts within the diatom assemblage, particularly favoring the largest species Guinardia striata. Other taxonomic groups contributed less to total phytoplankton biomass, but also displayed distinct responses to OA treatments. For instance, higher CO2 favored the occurrence of prymnesiophyceae (Phaeocystis globosa) and dictyochophyceae, whereas dinoflagellates were negatively affected by increasing CO2. Altogether, our findings revealed considerable shifts in species composition in response to elevated CO2 and indicated that phytoplankton communities in the subtropical oligotrophic oceans might be profoundly altered by ocean acidification.

Description: Oceanic uptake of anthropogenic carbon dioxide (CO2) causes pronounced shifts in marine carbonate chemistry and a decrease in seawater pH. Increasing evidence indicates that these changes—summarized by the term ocean acidification (OA)—can significantly affect marine food webs and biogeochemical cycles. However, current scientific knowledge is largely based on laboratory experiments with single species and artificial boundary conditions, whereas studies of natural plankton communities are still relatively rare. Moreover, the few existing community-level studies were mostly conducted in rather eutrophic environments, while less attention has been paid to oligotrophic systems such as the subtropical ocean gyres. Here we report from a recent in situ mesocosm experiment off the coast of Gran Canaria in the eastern subtropical North Atlantic, where we investigated the influence of OA on the ecology and biogeochemistry of plankton communities in oligotrophic waters under close-to-natural conditions. This paper is the first in this Research Topic of Frontiers in Marine Biogeochemistry and provides (1) a detailed overview of the experimental design and important events during our mesocosm campaign, and (2) first insights into the ecological responses of plankton communities to simulated OA over the course of the 62-day experiment. One particular scientific objective of our mesocosm experiment was to investigate how OA impacts might differ between oligotrophic conditions and phases of high biological productivity, which regularly occur in response to upwelling of nutrient-rich deep water in the study region. Therefore, we specifically developed a deep water collection system that allowed us to obtain ~85 m3 of seawater from ~650 m depth. Thereby, we replaced ~20% of each mesocosm's volume with deep water and successfully simulated a deep water upwelling event that induced a pronounced plankton bloom. Our study revealed significant effects of OA on the entire food web, leading to a restructuring of plankton communities that emerged during the oligotrophic phase, and was further amplified during the bloom that developed in response to deep water addition. Such CO2-related shifts in plankton community composition could have consequences for ecosystem productivity, biomass transfer to higher trophic levels, and biogeochemical element cycling of oligotrophic ocean regions.

Description: In the surface ocean, microorganisms are both a source of extracellular H2O2 and, via the production of H2O2 destroying enzymes, also one of the main H2O2 sinks. Within microbial communities, H2O2 sources and sinks may be unevenly distributed and thus microbial community structure could influence ambient extracellular H2O2 concentrations. Yet the biogeochemical cycling of H2O2 and other reactive oxygen species (ROS) is rarely investigated at the community level. Here, we present a time series of H2O2 concentrations during a 28-day mesocosm experiment where a pCO2 gradient (400–1,450 μatm) was applied to subtropical North Atlantic waters. Pronounced changes in H2O2 concentration were observed over the duration of the experiment. Initially H2O2 concentrations in all mesocosms were strongly correlated with surface H2O2 concentrations in ambient seawaters outside the mesocosms which ranged from 20 to 92 nM over the experiment duration (Spearman Rank Coefficients 0.79–0.93, p-values 〈 0.001–0.015). After approximately 9 days of incubation however, H2O2 concentrations had increased across all mesocosms, later reaching 〉300 nM in some mesocosms (2–6 fold higher than ambient seawaters). The correlation with ambient H2O2 was then no longer significant (p 〉 0.05) in all treatments. Furthermore, changes in H2O2 could not be correlated with inter-day changes in integrated irradiance. Yet H2O2 concentrations in most mesocosms were inversely correlated with bacterial abundance (negative Spearman Rank Coefficients ranging 0.59–0.94, p-values 〈 0.001–0.03). Our results therefore suggest that ambient H2O2 concentration can be influenced by microbial community structure with shifts toward high bacterial abundance correlated with low extracellular H2O2 concentrations. We also infer that the nature of mesocosm experiment design, i.e., the enclosure of water within open containers at the ocean surface, can strongly influence extracellular H2O2 concentrations. This has potential chemical and biological implications during incubation experiments due to the role of H2O2 as both a stressor to microbial functioning and a reactive component involved in the cycling of numerous chemical species including, for example, trace metals and haloalkanes.

Description: The subtropical oceans are home to one of the largest ecosystems on Earth, contributing to nearly one third of global oceanic primary production. Ocean warming leads to enhanced stratification in the oligotrophic ocean but also intensification in cross-shore wind gradients and thus in eddy kinetic energy across eastern boundary regions of the subtropical gyres. Phytoplankton thriving in a future warmer oligotrophic subtropical ocean with enhanced CO2 levels could therefore be patchily fertilized by increased mesoscale and submesoscale variability inducing nutrient pumping into the surface ocean. Under this premise, we have tested the response of three size classes (0.2-2, 2-20, and 〉 20 μm) of subtropical phytoplankton communities in terms of primary production, chlorophyll and cell biomass, to increasing CO2 concentrations and nutrient fertilization during an in situ mesocosm experiment in oligotrophic waters offof the island of Gran Canaria. We found no significant CO2-related effect on primary production and biomass under oligotrophic conditions (phase I). In contrast, primary production, chlorophyll and biomass displayed a significant and pronounced increase under elevated CO2 conditions in all groups after nutrient fertilization, both during the bloom (phase II) and post-bloom (phase III) conditions. Although the relative increase of primary production in picophytoplankton (250%) was 2.5 higher than in microphytoplankton (100%) after nutrient fertilization, comparing the high and low CO2 treatments, microphytoplankton dominated in terms of biomass, contributing 〉 57% to the total. These results contrast with similar studies conducted in temperate and cold waters, where consistently small phytoplankton benefitted after nutrient additions at high CO2, pointing to different CO2-sensitivities across plankton communities and ecosystem types in the ocean.

Description: The enzymatic electron transport system (ETS) assay is frequently used as a proxy of respiratory activity in planktonic communities. It is thought to estimate the maximum overall activity of the enzymes associated with the respiratory ETS systems in both eukaryotic and prokaryotic organisms. Thus, in order to derive actual respiration rates (R) from ETS it is necessary to determine empirical R/ETS conversion algorithms. In this study we explore the temporal development of R and ETS activity in natural plankton communities (from bacteria to large phytoplankton) enclosed in mesocosms, treated with different CO2 concentrations. The experiment lasted 30 days, during which abrupt changes in community structure and biomass occurred through a sharp transition from oligotrophy (phase I) to highly eutrophic conditions (phase II) after nutrient-induced fertilization (day 18). R and ETS did not show any response to CO2 under oligotrophic conditions, but R increased significantly more in the two high CO2 mesocosms after fertilization, coinciding with a sharp rise in large phytoplankton (mostly diatoms). R and ETS were significantly correlated only during the eutrophic phase. The R/ETS ranged more than threefold in magnitude during the experiment, with phase-averaged values significantly higher under oligotrophic conditions (0.7-1.1) than after nutrient fertilization (0.5-0.7). We did not find any significant relationship between R/ETS and community structure or biomass, although R correlated significantly with total biomass after fertilization in the four mesocosms. Multiple stepwise regression models show that large phytoplankton explains most of the variance in R during phases I (86%) and II (53%) and of ETS (86%) during phase II, while picophytoplankton contributes up to 73% to explain the variance in the ETS model during phase I. Our results suggest that R/ETS may be too variable in the ocean as to apply constant values to different communities living under contrasting environmental conditions. Controlled experiments with natural communities, like the present one, would help to constrain the range of variability of the R/ETS ratio, and to understand the factors driving it.

Description: Ocean acidification, the change in seawater carbonate chemistry due to the uptake of anthropogenic CO2, affects the physiology of marine organisms in multiple ways1. Diverse competitive and trophic interactions transform the metabolic responses to changes in community composition, seasonal succession and potentially geographical distribution of species. The health of ocean ecosystems depends on whether basic biotic functions are maintained, ecosystem engineers and keystone species are retained, and the spread of nuisance species is avoided2. Here, we show in a field experiment that the toxic microalga Vicicitus globosus has a selective advantage under ocean acidification, increasing its abundance in natural plankton communities at CO2 levels higher than 600 µatm and developing blooms above 800 µatm CO2. The mass development of V. globosus has had a dramatic impact on the plankton community, preventing the development of the micro- and mesozooplankton communities, thereby disrupting trophic transfer of primary produced organic matter. This has prolonged the residence of particulate matter in the water column and caused a strong decline in export flux. Considering its wide geographical distribution and confirmed role in fish kills3, the proliferation of V. globosus under the IPCC4 CO2 emission representative concentration pathway (RCP4.5 to RCP8.5) scenarios may pose an emergent threat to coastal communities, aquaculture and fisheries.

Description: Particulate matter in aquatic systems is an important vehicle for the transport of particulate organic carbon (POC). Its accurate measurement is of central importance for the understanding of marine carbon cycling. Previous work has shown that GF/F-filter-based bottle-sample-derived concentration estimates of POC are generally close to or higher than large-volume in-situ-pump-derived values (and in some rare cases in subzero waters are up to two orders of magnitude higher). To further investigate this phenomenon, water samples from the surface and mid-water Northeast Atlantic and the Baltic Sea were analyzed. Our data support a bias of POC concentration estimates caused by adsorption of nitrogen-rich dissolved organic material onto GF/F filters. For surface-ocean samples the mass per unit area of exposed filter and composition of adsorbed material depended on the filtered volume. Amounts of adsorbed OC were enhanced in the surface ocean (typically 0.5 μmol cm− 2 of exposed filter) as compared to the deep ocean (typically 0.2 μmol cm− 2 of exposed filter). These dependencies should be taken into account for future POC methodologies. Bottle/pump differences of samples that were not corrected for adsorption were higher in the deep ocean than in the surface ocean. This discrepancy increased in summer. It is shown that POC concentration estimates that were not corrected for adsorption depend not only on the filtered volume, true POC concentration and mass of adsorbed OC, but also on the filter area. However, in all cases we studied, correction for adsorption was important, but not sufficient, to explain bottle/pump differences. Artificial formation of filterable particles and/or processes leading to filterable material being lost from and/or missed by sample-processing procedures must be considered. It can be deduced that the maximum amounts of POC and particulate organic nitrogen (PON) that can be artificially formed per liter of filtered ocean water are ∼ 3–4 μM OC (5–10% of dissolved OC) and ∼ 0.2–0.5 μM ON (2–10% of dissolved ON), respectively. The relative sensitivities of bottle and pump procedures, and of surface- and deep-ocean material, to artificial particle formation and the missing/losing of material are evaluated. As present procedures do not exist to correct for all possible biasing effects due to artificial particle formation and/or miss/loss of filterable material, uncertainties of filtration-based estimates of POC concentrations need further testing. The challenge now is to further constrain the magnitude of the biasing effects that add to the adsorption effect to reduce the uncertainties of estimates of POC concentrations, inventories and fluxes in the ocean.

Description: The extracellular concentration of H2O2 in surface aquatic environments is controlled by a balance between photochemical production and the microbial synthesis of catalase and peroxidase enzymes to remove H2O2 from solution. In any kind of incubation experiment, the formation rates and equilibrium concentrations of reactive oxygen species (ROSs) such as H2O2 may be sensitive to both the experiment design, particularly to the regulation of incident light, and the abundance of different microbial groups, as both cellular H2O2 production and catalase–peroxidase enzyme production rates differ between species. Whilst there are extensive measurements of photochemical H2O2 formation rates and the distribution of H2O2 in the marine environment, it is poorly constrained how different microbial groups affect extracellular H2O2 concentrations, how comparable extracellular H2O2 concentrations within large-scale incubation experiments are to those observed in the surface-mixed layer, and to what extent a mismatch with environmentally relevant concentrations of ROS in incubations could influence biological processes differently to what would be observed in nature. Here we show that both experiment design and bacterial abundance consistently exert control on extracellular H2O2 concentrations across a range of incubation experiments in diverse marine environments. During four large-scale (〉1000 L) mesocosm experiments (in Gran Canaria, the Mediterranean, Patagonia and Svalbard) most experimental factors appeared to exert only minor, or no, direct effect on H2O2 concentrations. For example, in three of four experiments where pH was manipulated to 0.4–0.5 below ambient pH, no significant change was evident in extracellular H2O2 concentrations relative to controls. An influence was sometimes inferred from zooplankton density, but not consistently between different incubation experiments, and no change in H2O2 was evident in controlled experiments using different densities of the copepod Calanus finmarchicus grazing on the diatom Skeletonema costatum (〈1 % change in [H2O2] comparing copepod densities from 1 to 10 L−1). Instead, the changes in H2O2 concentration contrasting high- and low-zooplankton incubations appeared to arise from the resulting changes in bacterial activity. The correlation between bacterial abundance and extracellular H2O2 was stronger in some incubations than others (R2 range 0.09 to 0.55), yet high bacterial densities were consistently associated with low H2O2. Nonetheless, the main control on H2O2 concentrations during incubation experiments relative to those in ambient, unenclosed waters was the regulation of incident light. In an open (lidless) mesocosm experiment in Gran Canaria, H2O2 was persistently elevated (2–6-fold) above ambient concentrations; whereas using closed high-density polyethylene mesocosms in Crete, Svalbard and Patagonia H2O2 within incubations was always reduced (median 10 %–90 %) relative to ambient waters.