Ocean acidification alters microeukaryotic and bacterial food web interactions in a eutrophic subtropical mesocosm.

Ocean acidification (OA) is known to influence biological and ecological processes, mainly focusing on its impacts on single species, but little has been documented on how OA may alter plankton community interactions. Here, we conducted a mesocosm experiment with ambient (∼410 ppmv) and high (1000 ppmv) CO2 concentrations in a subtropical eutrophic region of the East China Sea and examined the community dynamics of microeukaryotes, bacterioplankton and microeukaryote-attached bacteria in the enclosed coastal seawater. The OA treatment with elevated CO2 affected taxa as the phytoplankton bloom stages progressed, with a 72.89% decrease in relative abundance of the protist Cercozoa on day 10 and a 322% increase in relative abundance of Stramenopile dominated by diatoms, accompanied by a 29.54% decrease in relative abundance of attached Alphaproteobacteria on day 28. Our study revealed that protozoans with different prey preferences had differing sensitivity to high CO2, and attached bacteria were more significantly affected by high CO2 compared to bacterioplankton. Our findings indicate that high CO2 changed the co-occurrence network complexity and stability of microeukaryotes more than those of bacteria. Furthermore, high CO2 was found to alter the proportions of potential interactions between phytoplankton and their predators, as well as microeukaryotes and their attached bacteria in the networks. The changes in the relative abundances and interactions of microeukaryotes between their predators in response to high CO2 revealed in our study suggest that high CO2 may have profound impacts on marine food webs.

Light history modulates growth and photosynthetic responses of a diatom to ocean acidification and UV radiation.

To examine the synergetic effects of ocean acidification (OA) and light intensity on the photosynthetic performance of marine diatoms, the marine centric diatom Thalassiosira weissflogii was cultured under ambient low CO2 (LC, 390 µatm) and elevated high CO2 (HC, 1000 µatm) levels under low-light (LL, 60 µmol m-2 s-1) or high-light (HL, 220 µmol m-2 s-1) conditions for over 20 generations. HL stimulated the growth rate by 128 and 99% but decreased cell size by 9 and 7% under LC and HC conditions, respectively. However, HC did not change the growth rate under LL but decreased it by 9% under HL. LL combined with HC decreased both maximum quantum yield (F V/F M) and effective quantum yield (Φ PSII), measured under either low or high actinic light. When exposed to UV radiation (UVR), LL-grown cells were more prone to UVA exposure, with higher UVA and UVR inducing inhibition of Φ PSII compared with HL-grown cells. Light use efficiency (α) and maximum relative electron transport rate (rETRmax) were inhibited more in the HC-grown cells when UVR (UVA and UVB) was present, particularly under LL. Our results indicate that the growth light history influences the cell growth and photosynthetic responses to OA and UVR. Supplementary Information: The online version contains supplementary material available at 10.1007/s42995-022-00138-x.

Enhancement of diatom growth and phytoplankton productivity with reduced O2 availability is moderated by rising CO2.

Many marine organisms are exposed to decreasing O2 levels due to warming-induced expansion of hypoxic zones and ocean deoxygenation (DeO2). Nevertheless, effects of DeO2 on phytoplankton have been neglected due to technical bottlenecks on examining O2 effects on O2-producing organisms. Here we show that lowered O2 levels increased primary productivity of a coastal phytoplankton assemblage, and enhanced photosynthesis and growth in the coastal diatom Thalassiosira weissflogii. Mechanistically, reduced O2 suppressed mitochondrial respiration and photorespiration of T. weissflogii, but increased the efficiency of their CO2 concentrating mechanisms (CCMs), effective quantum yield and improved light use efficiency, which was apparent under both ambient and elevated CO2 concentrations leading to ocean acidification (OA). While the elevated CO2 treatment partially counteracted the effect of low O2 in terms of CCMs activity, reduced levels of O2 still strongly enhanced phytoplankton primary productivity. This implies that decreased availability of O2 with progressive DeO2 could boost re-oxygenation by diatom-dominated phytoplankton communities, especially in hypoxic areas, with potentially profound consequences for marine ecosystem services in coastal and pelagic oceans.

Elevated pCO2 changes community structure and function by affecting phytoplankton group-specific mortality.

The rise of atmospheric pCO2 has created a number of problems for marine ecosystem. In this study, we initially quantified the effects of elevated pCO2 on the group-specific mortality of phytoplankton in a natural community based on the results of mesocosm experiments. Diatoms dominated the phytoplankton community, and the concentration of chlorophyll a was significantly higher in the high-pCO2 treatment than the low-pCO2 treatment. Phytoplankton mortality (percentage of dead cells) decreased during the exponential growth phase. Although the mortality of dinoflagellates did not differ significantly between the two pCO2 treatments, that of diatoms was lower in the high-pCO2 treatment. Small diatoms dominated the diatom community. Although the mortality of large diatoms did not differ significantly between the two treatments, that of small diatoms was lower in the high-pCO2 treatment. These results suggested that elevated pCO2 might enhance dominance by small diatoms and thereby change the community structure of coastal ecosystems.

Ocean acidification interacts with variable light to decrease growth but increase particulate organic nitrogen production in a diatom.

Phytoplankton in the upper oceans are exposed to changing light levels due to mixing, diurnal solar cycles and weather conditions. Consequently, effects of ocean acidification are superimposed upon responses to variable light levels. We therefore grew a model diatom Thalassiosira pseudonana under either constant or variable light but at the same daily photon dose, with current low (400 µatm, LC) and future high CO2 (1000 µatm, HC) treatments. Variable light, compared with the constant light regime, decreased the growth rate, Chl a, Chl c, and carotenoid contents under both LC and HC conditions. Cells grown under variable light appeared more tolerant of high light as indicated by higher maximum relative electron transport rate and saturation light. Light variation interacted with high CO2/lowered pH to decrease the carbon fixation rate, but increased particulate organic carbon (POC) and particularly nitrogen (PON) per cell, which drove a decrease in C/N ratio, reflecting changes in the efficiency of energy transfer from photo-chemistry to net biomass production. Our results imply that elevated pCO2 under varying light conditions can lead to less primary productivity but more PON per biomass of the diatom, which might improve the food quality of diatoms and thereby influence biogeochemical nitrogen cycles.

Functional responses of smaller and larger diatoms to gradual CO2 rise.

Diatoms and other phytoplankton groups are exposed to abrupt changes in pCO2, in waters in upwelling areas, near CO2 seeps, or during their blooms; or to more gradual pCO2 rise through anthropogenic CO2 emissions. Gradual CO2 rises have, however, rarely been included in ocean acidification (OA) studies. We therefore compared how small (Thalassiosira pseudonana) and larger (Thalassiosira weissflogii) diatom cell isolates respond to gradual pCO2 rises from 180 to 1000 µatm in steps of ~40 µatm with 5-10 generations at each step, and whether their responses to gradual pCO2 rise differ when compared to an abrupt pCO2 rise imposed from ambient 400 directly to 1000 µatm. Cell volume increased in T. pseudonana but decreased in T. weissflogii with an increase from low to moderate CO2 levels, and then remained steady under yet higher CO2 levels. Growth rates were stimulated, but Chl a, particulate organic carbon (POC) and cellular biogenic silica (BSi) decreased from low to moderate CO2 levels, and then remained steady with further CO2 rise in both species. Decreased saturation light intensity (Ik) and light use efficiency (α) with CO2 rise in T. pseudonana indicate that the smaller diatom becomes more susceptible to photoinhibition. Decreased BSi/POC (Si/C) in T. weissflogii indicates the biogeochemical cycles of both silicon and carbon may be more affected by elevated pCO2 in the larger diatom. The different CO2 modulation methods resulted in different responses of some key physiological parameters. Increasing pCO2 from 180 to 400 µatm decreased cellular POC and BSi contents, implying that ocean acidification to date has already altered diatom contributions to carbon and silicon biogeochemical processes.

Insensitivities of a subtropical productive coastal plankton community and trophic transfer to ocean acidification: Results from a microcosm study.

Ocean acidification (OA) has potential to affect marine phytoplankton in ways that are partly understood, but there is less knowledge about how it may alter the coupling to secondary producers. We investigated the effects of OA on phytoplankton primary production, and its trophic transfer to zooplankton in a subtropical eutrophic water (Wuyuan Bay, China) under present day (400 µatm) and projected end-of-century (1000 µatm) pCO2 levels. Net primary production was unaffected, although OA did lead to small decreases in growth rates. OA had no measurable effect on micro-/mesozooplankton grazing rates. Elevated pCO2 had no effect on phytoplankton fatty acid (FA) concentrations during exponential phase, but saturated FAs increased relative to the control during declining phase. FA profiles of mesozooplankton were unaffected. Our findings show that short-term exposure of plankton communities in eutrophic subtropical waters to projected end-of-century OA conditions has little effect on primary productivity and trophic linkage to mesozooplankton.

Rising levels of temperature and CO2 antagonistically affect phytoplankton primary productivity in the South China Sea.

Coastal and offshore waters in the South China Sea are warming and becoming acidified due to rising atmospheric levels of carbon dioxide (CO2), yet the combined effects of these two stressors are poorly known. Here, we carried out shipboard incubations at ambient (398 µatm) and elevated (934 µatm) pCO2 at in situ and in situ+1.8 °C temperatures and we measured primary productivity at two coastal and two offshore stations. Both warming and increased CO2 levels individually increased phytoplankton productivity at all stations, but the combination of high temperature and high CO2 did not, reflecting an antagonistic effect. Warming decreased Chl a concentrations in off-shore waters at ambient CO2, but had no effect in the coastal waters. The high CO2 treatment increased night time respiration in the coastal waters at ambient temperatures. Our findings show that phytoplankton assemblage responses to rising temperature and CO2 levels differ between coastal and offshore waters. While it is difficult to predict how ongoing warming and acidification will influence primary productivity in the South China Sea, our data imply that predicted increases in temperature and pCO2 will not boost surface phytoplankton primary productivity.

The fatty acid content of plankton is changing in subtropical coastal waters as a result of OA: Results from a mesocosm study.

Ocean Acidification (OA) effects on marine plankton are most often considered in terms of inorganic carbon chemistry, but decreasing pH may influence other aspects of cellular metabolism. Here we present the effects of OA on the fatty acid (FA) content and composition of an artificial phytoplankton community (Phaeodactylum tricornutum, Thalassiosira weissflogii, and Emiliania huxleyi) in a fully replicated, ∼4 m3 mesocosm study in subtropical coastal waters (Wuyuan Bay, China, 24.52°N, 117.18°E) at present day (400 µatm) and elevated (1000 µatm) pCO2 concentrations. Phytoplankton growth occurred in three phases during the 33-day experiment: an initial exponential growth leading to senescence and a subsequent decline phase. Phytoplankton sampled from these mesocosms were fed to mesozooplankton collected by net haul from Wuyuan Bay. Concentrations of saturated fatty acids (SFA) in both phytoplankton and mesozooplankton remained high under acidified and non-acidified conditions. However, polyunsaturated fatty acids (PUFA) and monounsaturated fatty acids (MUFA) increased significantly more under elevated pCO2 during the late exponential phase (Day 13), indicating increased nutritional value for zooplankton and higher trophic levels. Indeed, uptake rates of the essential FA docosahexaenoic acid (C20:5n3, DHA) increased in mesozooplankton under acidified conditions. However, mesozooplankton grazing rates decreased overall with elevated pCO2. Our findings show that these selected phytoplankton species have a relatively high tolerance to acidification in terms of FA production, and local mesozooplankton in these subtropical coastal waters can maintain their FA composition under end of century ocean acidification conditions.

Carbon assimilation and losses during an ocean acidification mesocosm experiment, with special reference to algal blooms.

A mesocosm experiment was conducted in Wuyuan Bay (Xiamen), China, to investigate the effects of elevated pCO2 on bloom formation by phytoplankton species previously studied in laboratory-based ocean acidification experiments, to determine if the indoor-grown species performed similarly in mesocosms under more realistic environmental conditions. We measured biomass, primary productivity and particulate organic carbon (POC) as well as particulate organic nitrogen (PON). Phaeodactylum tricornutum outcompeted Thalassiosira weissflogii and Emiliania huxleyi, comprising more than 99% of the final biomass. Mainly through a capacity to tolerate nutrient-limited situations, P. tricornutum showed a powerful sustained presence during the plateau phase of growth. Significant differences between high and low CO2 treatments were found in cell concentration, cumulative primary productivity and POC in the plateau phase but not during the exponential phase of growth. Compared to the low pCO2 (LC) treatment, POC increased by 45.8-101.9% in the high pCO2 (HC) treated cells during the bloom period. Furthermore, respiratory carbon losses of gross primary productivity were found to comprise 39-64% for the LC and 31-41% for the HC mesocosms (daytime C fixation) in phase II. Our results suggest that the duration and characteristics of a diatom bloom can be affected by elevated pCO2. Effects of elevated pCO2 observed in the laboratory cannot be reliably extrapolated to large scale mesocosms with multiple influencing factors, especially during intense algal blooms.

Ocean acidification increases the accumulation of toxic phenolic compounds across trophic levels.

Increasing atmospheric CO2 concentrations are causing ocean acidification (OA), altering carbonate chemistry with consequences for marine organisms. Here we show that OA increases by 46-212% the production of phenolic compounds in phytoplankton grown under the elevated CO2 concentrations projected for the end of this century, compared with the ambient CO2 level. At the same time, mitochondrial respiration rate is enhanced under elevated CO2 concentrations by 130-160% in a single species or mixed phytoplankton assemblage. When fed with phytoplankton cells grown under OA, zooplankton assemblages have significantly higher phenolic compound content, by about 28-48%. The functional consequences of the increased accumulation of toxic phenolic compounds in primary and secondary producers have the potential to have profound consequences for marine ecosystem and seafood quality, with the possibility that fishery industries could be influenced as a result of progressive ocean changes.

Temperature relations of aerial and aquatic physiological performance in a mid-intertidal limpet Cellana toreuma: adaptation to rapid changes in thermal stress during emersion.

The physiological performance of a mid-intertidal limpet Cellana toreuma was determined to study the physiological adaptation of intertidal animals to rapid changes and extreme temperatures during emersion. The relationship between the Arrhenius breakpoint temperature (ABT) and in situ operative body temperature was studied to predict the possible impact of climate change on the species. The temperature coefficient (Q10) of emersed animals was higher than that of submersed animals and the ratio of aerial: aquatic heart rate rose with increasing temperature. The ABTs of submersed and emersed animals were 30.2 and 34.2°C, respectively. The heart rate and levels of molecular biomarkers (hsps, ampkα, ampkß and sirt1 mRNA) were determined in 48 h simulated semi-diurnal tides. There were no obvious changes of heart rate and gene expression during the transition between emersion and submersion at room temperature, although expressions of hsp70 and hsp90 were induced significantly after thermal stress. These results indicate that C. toreuma can effectively utilize atmospheric oxygen, and the higher Q10 and ABT of emersed animals are adaptations to the rapid change and extreme thermal stress during emersion. However, the in situ operative body temperature frequently exceeds the aerial ABT of C. toreuma, indicating the occurrence of large-scale mortality of C. toreuma in summer, and this species should be sensitive to increasing temperature in the scenario of climate change.