Correlation of methane production with physiological traits in Trichodesmium IMS 101 grown with methylphosphonate at different temperatures.

The diazotrophic cyanobacterium Trichodesmium has been recognized as a potentially significant contributor to aerobic methane generation via several mechanisms including the utilization of methylphophonate (MPn) as a source of phosphorus. Currently, there is no information about how environmental factors regulate methane production by Trichodesmium. Here, we grew Trichodesmium IMS101 at five temperatures ranging from 16 to 31°C, and found that its methane production rates increased with rising temperatures to peak (1.028 ± 0.040 nmol CH4 µmol POC-1 day-1) at 27°C, and then declined. Its specific growth rate changed from 0.03 ± 0.01 d-1 to 0.34 ± 0.02 d-1, with the optimal growth temperature identified between 27 and 31°C. Within the tested temperature range the Q10 for the methane production rate was 4.6 ± 0.7, indicating a high sensitivity to thermal changes. In parallel, the methane production rates showed robust positive correlations with the assimilation rates of carbon, nitrogen, and phosphorus, resulting in the methane production quotients (molar ratio of carbon, nitrogen, or phosphorus assimilated to methane produced) of 227-494 for carbon, 40-128 for nitrogen, and 1.8-3.4 for phosphorus within the tested temperature range. Based on the experimental data, we estimated that the methane released from Trichodesmium can offset about 1% of its CO2 mitigation effects.

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.

Ocean acidification and desalination increase the growth and photosynthesis of the diatom Skeletonema costatum isolated from the coastal water of the Yellow Sea.

Global climate changes induce substantial alterations in the marine system, including ocean acidification (OA), desalination and warming of surface seawater. Here, we examined the combined effects of OA and reduced salinity under different temperatures on the growth and photosynthesis of the diatom Skeletonema costatum. After having been acclimated to 2 CO2 concentrations (400 µatm, 1000 µatm) and 2 salinity levels (20 psu, 30 psu) at temperature levels of 10 °C and 20 °C, the diatom showed enhanced growth rate at the lowered salinity and elevated pCO2 irrespective of the temperature. The OA treatment increased the net photosynthetic rate and biogenic silica (Bsi) contents. Increasing the temperature from 10 to 20 °C raised the net photosynthetic rate by over twofold. The elevated pCO2 increased the net and gross photosynthetic rates by 20%-40% and by 16%-32%, respectively, with the higher enhancement observed at the higher levels of salinity and temperature. Our results imply that OA and desalination along with warming to the levels tested can enhance S. costatum's competitiveness in coastal phytoplankton communities under influence of future climate changes.

UV-A radiation increases biomass yield by enhancing energy flow and carbon assimilation in the edible cyanobacterium Nostoc sphaeroides.

Ultraviolet (UV) A radiation (315-400 nm) is the predominant component of solar UV radiation that reaches the Earth's surface. However, the underlying mechanisms of the positive effects of UV-A on photosynthetic organisms have not yet been elucidated. In this study, we investigated the effects of UV-A radiation on the growth, photosynthetic ability, and metabolome of the edible cyanobacterium Nostoc sphaeroides. Exposures to 5-15 W m-2 (15-46 µmol photons m-2 s-1) UV-A and 4.35 W m-2 (20 µmol photons m-2 s-1) visible light for 16 days significantly increased the growth rate and biomass production of N. sphaeroides cells by 18%-30% and 15%-56%, respectively, compared to the non-UV-A-acclimated cells. Additionally, the UV-A-acclimated cells exhibited a 1.8-fold increase in the cellular nicotinamide adenine dinucleotide phosphate (NADP) pool with an increase in photosynthetic capacity (58%), photosynthetic efficiency (24%), QA re-oxidation, photosystem I abundance, and cyclic electron flow (87%), which further led to an increase in light-induced NADPH generation (31%) and ATP content (83%). Moreover, the UV-A-acclimated cells showed a 2.3-fold increase in ribulose-1,5-bisphosphate carboxylase/oxygenase activity, indicating an increase in their carbon-fixing capacity. Gas chromatography-mass spectrometry-based metabolomics further revealed that UV-A radiation upregulated the energy-storing carbon metabolism, as evidenced by the enhanced accumulation of sugars, fatty acids, and citrate in the UV-A-acclimated cells. Therefore, our results demonstrate that UV-A radiation enhances energy flow and carbon assimilation in the cyanobacterium N. sphaeroides.IMPORTANCEUltraviolet (UV) radiation exerts harmful effects on photo-autotrophs; however, several studies demonstrated the positive effects of UV radiation, especially UV-A radiation (315-400 nm), on primary productivity. Therefore, understanding the underlying mechanisms associated with the promotive effects of UV-A radiation on primary productivity can facilitate the application of UV-A for CO2 sequestration and lead to the advancement of photobiological sciences. In this study, we used the cyanobacterium Nostoc sphaeroides, which has an over 1,700-year history of human use as food and medicine, to explore its photosynthetic acclimation response to UV-A radiation. As per our knowledge, this is the first study to demonstrate that UV-A radiation increases the biomass yield of N. sphaeroides by enhancing energy flow and carbon assimilation. Our findings provide novel insights into UV-A-mediated photosynthetic acclimation and provide a scientific basis for the application of UV-A radiation for optimizing light absorption capacity and enhancing CO2 sequestration in the frame of a future CO2 neutral, circular, and sustainable bioeconomy.

Warming exacerbates the impacts of ultraviolet radiation in temperate diatoms but alleviates the effect on polar species.

Under global change scenarios, the sea surface temperature is increasing steadily along with other changes to oceanic environments. Consequently, marine diatoms are influenced by multiple ocean global change drivers. We hypothesized that temperature rise mediates the responses of polar and temperate diatoms to UV radiation (UVR) to different extents, and exposed the temperate centric diatoms, Thalassiosira weissflogii and Skeletonema costatum, and a polar pennate diatom Entomoneis sp., to warming (+5°C) for 10 days, then performed short-term incubations under different radiation treatments with or without UVR. The effective quantum yields of the three diatoms were stable during exposure to PAR, but decreased when exposed to PAR + UVR, leading to significant UV-induced inhibition, which was 3% and 9%, respectively, for T. weissflogii and S. costatum under ambient temperature but increased to 12% and 17%, respectively, in the cells acclimated to the warming treatment. In contrast, UVR induced much higher inhibition, by about 45%, in the polar diatom Entomoneis sp. at ambient temperature, and the warming treatment alleviated the UV-induced inhibition, which dropped to 36%. The growth rates were significantly inhibited by UVR in S. costatum under the warming treatment and in Entomoneis sp. under ambient temperature, while there was no significant effect for T. weissflogii. Our results indicate that the polar diatom was more sensitive to UVR though warming could alleviate its impact, whereas the temperate diatoms were less sensitive to UVR but warming exacerbated its impacts, implying that diatoms living in different regions may exhibit differential responses to global changes.

Shift in algal blooms from micro- to macroalgae around China with increasing eutrophication and climate change.

Blooms of microalgal red tides and macroalgae (e.g., green and golden tides caused by Ulva and Sargassum) have caused widespread problems around China in recent years, but there is uncertainty around what triggers these blooms and how they interact. Here, we use 30 years of monitoring data to help answer these questions, focusing on the four main species of microalgae Prorocentrum donghaiense, Karenia mikimotoi, Noctiluca scintillans, and Skeletonema costatum) associated with red tides in the region. The frequency of red tides increased from 1991 to 2003 and then decreased until 2020, with S. costatum red tides exhibiting the highest rate of decrease. Green tides started to occur around China in 1999 and the frequency of green tides has since been on the increase. Golden tides were first reported to occur around China in 2012. The frequency of macroalgal blooms has a negative linear relationship with the frequency and coverage of red tides around China, and a positive correlation with total nitrogen and phosphorus loads as well as with atmospheric CO2 and sea surface temperature (SST). Increased outbreaks of macroalgal blooms are very likely due to worsening levels of eutrophication, combined with rising CO2 and SST, which contribute to the reduced frequency of red tides. The increasing grazing rate of microzooplankton also results in the decline in areas affected by red tides. This study shows a clear shift of algal blooms from microalgae to macroalgae around China over the past 30 years driven by the combination of eutrophication, climate change, and grazing stress, indicating a fundamental change in coastal systems in the region.

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.

Deoxygenation enhances photosynthetic performance and increases N2 fixation in the marine cyanobacterium Trichodesmium under elevated pCO2.

Effects of changed levels of dissolved O2 and CO2 on marine primary producers are of general concern with respect to ecological effects of ongoing ocean deoxygenation and acidification as well as upwelled seawaters. We investigated the response of the diazotroph Trichodesmium erythraeum IMS 101 after it had acclimated to lowered pO2 (~60 µM O2) and/or elevated pCO2 levels (HC, ~32 µM CO2) for about 20 generations. Our results showed that reduced O2 levels decreased dark respiration significantly, and increased the net photosynthetic rate by 66 and 89% under the ambient (AC, ~13 µM CO2) and the HC, respectively. The reduced pO2 enhanced the N2 fixation rate by ~139% under AC and only by 44% under HC, respectively. The N2 fixation quotient, the ratio of N2 fixed per O2 evolved, increased by 143% when pO2 decreased by 75% under the elevated pCO2. Meanwhile, particulate organic carbon and nitrogen quota increased simultaneously under reduced O2 levels, regardless of the pCO2 treatments. Nevertheless, changed levels of O2 and CO2 did not bring about significant changes in the specific growth rate of the diazotroph. Such inconsistency was attributed to the daytime positive and nighttime negative effects of both lowered pO2 and elevated pCO2 on the energy supply for growth. Our results suggest that Trichodesmium decrease its dark respiration by 5% and increase its N2-fixation by 49% and N2-fixation quotient by 30% under future ocean deoxygenation and acidification with 16% decline of pO2 and 138% rise of pCO2 by the end of this century.

Increased genetic diversity loss and genetic differentiation in a model marine diatom adapted to ocean warming compared to high CO2.

Although high CO2 and warming could act interactively on marine phytoplankton, little is known about the molecular basis for this interaction on an evolutionary scale. Here we explored the adaptation to high CO2 in combination with warming in a model marine diatom Phaeodactylum tricornutum. Whole-genome re-sequencing identifies, in comparison to populations grown under control conditions, a larger genetic diversity loss and a higher genetic differentiation in the populations adapted for 2 years to warming than in those adapted to high CO2. However, this diversity loss was less under high CO2 combined with warming, suggesting that the evolution driven by warming was constrained by high CO2. By integrating genomics, transcriptomics, and physiological data, we found that the underlying molecular basis for this constraint is associated with the expression of genes involved in some key metabolic pathways or biological processes, such as the glyoxylate pathway, amino acid and fatty acid metabolism, and diel variability. Our results shed new light on the evolutionary responses of marine phytoplankton to multiple environmental changes in the context of global change and provide new insights into the molecular basis underpinning interactions among those multiple drivers.

Corrigendum: Applying Dialysis Bags to Grow Microalgae and Measure Grazing Rates by Secondary Producers.

[This corrects the article DOI: 10.3389/fphys.2022.838001.].

Applying Dialysis Bags to Grow Microalgae and Measure Grazing Rates by Secondary Producers.

Traditional methods using sealed bottles to determine the grazing rates by secondary producers neglect chemical changes induced by biological activities during the incubation, giving rise to instable levels of nutrients, pH, pCO2, pO2 and other chemicals along with changing microalgal cell concentrations and grazers' metabolism. Here, we used dialysis bags, which allows exchanges of nutrients and gases, to grow microalgae and to determine grazing rates of secondary producers. The specific growth rate of diatom within the dialysis bags increased with increasing water velocities, indicating its suitability to grow microalgae under dynamic water conditions. Then, we compared the grazing rates by the heterotrophic dinoflagellate Noctiluca scintillans measured with the traditional method using polycarbonate (PC) bottles and the approach with the dialysis bags, and found that these two methods gave rise to comparable grazing rates. Nevertheless, the concentrations of inorganic nitrogen and phosphate in the closed PC bottles were about 89-94% lower than those in the dialysis bags due to the microalga's assimilation. Subsequently, we applied it to determine the grazing rates by a copepod and an oyster (in the presence of other grazers). Consistent results were obtained using the dialysis bags to determine grazing rates by copepods. During the mesocosm (3000 L) experiment in the presence of primary and secondary producers, the grazing rates by the oyster Crassostrea angulata were determined based on the difference of phytoplankton biomass within and outside of the dialysis bags that held all organisms in the mesocosm except the oyster. Since the dialysis bags are permeable to gases, the grazing rates by the oyster under 410 (AC) and 1,000 (HC) µatm CO2 were successfully measured, with a promising result that HC significantly increased the oyster's grazing. We concluded that using dialysis bags to grow microalgae and to determine grazing rates is a reliable approach, especially under different levels of CO2 and O2.

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.

Additive impacts of ocean acidification and ambient ultraviolet radiation threaten calcifying marine primary producers.

Ocean acidification (OA) represents a threat to marine organisms and ecosystems. However, OA rarely exists in isolation but occurs concomitantly with other stressors such as ultraviolet radiation (UVR), whose effects have been neglected in oceanographical observations. Here, we perform a quantitative meta-analysis based on 373 published experimental assessments from 26 studies to examine the combined effects of OA and UVR on marine primary producers. The results reveal predominantly additive stressor interactions (69-84% depending on the UV waveband), with synergistic and antagonistic interactions being rare but significantly different between micro- and macro-algae. In microalgae, variations in interaction type frequencies are related to cell volume, with antagonistic interactions accounting for a higher proportion in larger sized species. Despite additive interactions being most frequent, the small proportion of antagonistic interactions appears to have a stronger power, leading to neutral effects of OA in combination with UVR. High levels of UVR at near in situ conditions in combination with OA showed additive inhibition of calcification, but not when UVR was low. The results also reveal that the magnitude of responses is strongly dependent on experimental duration, with the negative effects of OA on calcification and pigmentation being buffered and amplified by increasing durations, respectively. Tropical primary producers were more vulnerable to OA or UVR alone compared to conspecifics from other climatic regions. Our analysis highlights that further multi-stressor long-term adaptation experiments with marine organisms of different cell volumes (especially microalgae) from different climatic regions are needed to fully disclose future impacts of OA and UVR.

Nitrogen-limitation exacerbates the impact of ultraviolet radiation on the coccolithophore Gephyrocapsa oceanica.

To investigate effects of UV radiation (UVR, 280-400 nm) on coccolithophorids under nutrient-limited conditions, we grew Gephyrocapsa oceanica to determine its resilience to consecutive daily short-term exposures to +UVR (irradiances >295 nm) under a range of nitrate availabilities (100, 24, 12, 6 and 3 µM). +UVR alone significantly hampered the growth of G. oceanica, with the synergistic negative effects of +UVR and N-limitation being about 58% and 22% greater than under UVR or N-limitation alone, respectively. Most 3 µM nitrate cultures died, but those exposed to UVR succumbed sooner. This was due to a failure of photoprotection and repair mechanisms under low N-availability with exposures to UVR. Additionally, the UVR-induced inhibition of the effective quantum yield of photosystem II (PSII) was significantly higher and was further aggravated by N limitation. The algal cells increased photoprotective pigments and UV-absorbing compounds as a priority rather than using calcification for defense against UVR, indicating a trade-off in energy and resource allocation. Our results indicate the negative effects of UVR on coccolithophorid growth and photosynthesis, and highlight the important role of N availability in defense against UVR as well as high PAR. We predict that enhanced N-limitation in future surface oceans due to warming-induced stratification will exacerbate the sensitivity of G. oceanica to UVR, while coccolithophores can be potentially more susceptible to other environmental stresses due to increased levels of nutrient limitation.

Increased CO2 Relevant to Future Ocean Acidification Alleviates the Sensitivity of a Red Macroalgae to Solar Ultraviolet Irradiance by Modulating the Synergy Between Photosystems II and I.

While intertidal macroalgae are exposed to drastic changes in solar photosynthetically active radiation (PAR) and ultraviolet radiation (UVR) during a diel cycle, and to ocean acidification (OA) associated with increasing CO2 levels, little is known about their photosynthetic performance under the combined influences of these drivers. In this work, we examined the photoprotective strategies controlling electron flow through photosystems II (PSII) and photosystem I (PSI) in response to solar radiation with or without UVR and an elevated CO2 concentration in the intertidal, commercially important, red macroalgae Pyropia (previously Porphyra) yezoensis. By using chlorophyll fluorescence techniques, we found that high levels of PAR alone induced photoinhibition of the inter-photosystem electron transport carriers, as evidenced by the increase of chlorophyll fluorescence in both the J- and I-steps of Kautsky curves. In the presence of UVR, photoinduced inhibition was mainly identified in the O2-evolving complex (OEC) and PSII, as evidenced by a significant increase in the variable fluorescence at the K-step (F k) of Kautsky curves relative to the amplitude of F J-F o (Wk) and a decrease of the maximum quantum yield of PSII (F v/F m). Such inhibition appeared to ameliorate the function of downstream electron acceptors, protecting PSI from over-reduction. In turn, the stable PSI activity increased the efficiency of cyclic electron transport (CET) around PSI, dissipating excess energy and supplying ATP for CO2 assimilation. When the algal thalli were grown under increased CO2 and OA conditions, the CET activity became further enhanced, which maintained the OEC stability and thus markedly alleviating the UVR-induced photoinhibition. In conclusion, the well-established coordination between PSII and PSI endows P. yezoensis with a highly efficient photochemical performance in response to UVR, especially under the scenario of future increased CO2 levels and OA.

Ocean acidification exacerbates copper toxicity in both juvenile and adult stages of the green tide alga Ulva linza.

The toxicity of heavy metals to coastal organisms can be modulated by changes in pH due to progressive ocean acidification (OA). We investigated the combined impacts of copper and OA on different stages of the green macroalga Ulva linza, which is widely distributed in coastal waters, by growing the alga under the addition of Cu (control, 0.125 (medium, MCu), and 0.25 (high) µM, HCu) and elevated pCO2 of 1,000 µatm, predicted in the context of global change. The relative growth rates decreased significantly in both juvenile and adult thalli at HCu under OA conditions. The net photosynthetic and respiration rates, as well as the relative electron transfer rates for the adult thalli, also decreased under the combined impacts of HCu and OA, although no significant changes in the contents of photosynthetic pigments were detected. Our results suggest that Cu and OA act synergistically to reduce the growth and photosynthetic performance of U. linza, potentially prolonging its life cycle.

Effects of climate change factors on marine macroalgae: A review.

Marine macroalgae, the main primary producers in coastal waters, play important roles in the fishery industry and global carbon cycles. With progressive ocean global changes, however, they are increasingly exposed to enhanced levels of multiple environmental drivers, such as ocean acidification, warming, heatwaves, UV radiation and deoxygenation. While most macroalgae have developed physiological strategies against variations of these drivers, their eco-physiological responses to each or combinations of the drivers differ spatiotemporally and species-specifically. Many freshwater macroalgae are tolerant of pH drop and its diel fluctuations and capable of acclimating to changes in carbonate chemistry. However, calcifying species, such as coralline algae, are very sensitive to acidification of seawater, which reduces their calcification, and additionally, temperature rise and UV further decrease their physiological performance. Except for these calcifying species, both economically important and harmful macroalgae can benefit from elevated CO2 concentrations and moderate temperature rise, which might be responsible for increasing events of harmful macroalgal blooms including green macroalgal blooms caused by Ulva spp. and golden tides caused by Sargassum spp. Upper intertidal macroalgae, especially those tolerant of dehydration during low tide, increase their photosynthesis under elevated CO2 concentrations during the initial dehydration period, however, these species might be endangered by heatwaves, which can expose them to high temperature levels above their thermal windows' upper limit. On the other hand, since macroalgae are distributed in shallow waters, they are inevitably exposed to solar UV radiation. The effects of UV radiation, depending on weather conditions and species, can be harmful as well as beneficial to many species. Moderate levels of UV-A (315-400nm) can enhance photosynthesis of green, brown and red algae, while UV-B (280-315nm) mainly show inhibitory impacts. Although little has been documented on the combined effects of elevated CO2, temperature or heatwaves with UV radiation, exposures to heatwaves during midday under high levels of UV radiation can be detrimental to most species, especially to their microscopic stages which are less tolerant of climate change induced stress. In parallel, reduced availability of dissolved O2 in coastal water along with eutrophication might favour the macroalgae's carboxylation process by suppressing their oxygenation or photorespiration. In this review, we analyse effects of climate change-relevant drivers individually and/or jointly on different macroalgal groups and different life cycle stages based on the literatures surveyed, and provide perspectives for future studies.

Ultraviolet Radiation Stimulates Activity of CO2 Concentrating Mechanisms in a Bloom-Forming Diatom Under Reduced CO2 Availability.

The diatom Skeletonema costatum is cosmopolitan and forms algal blooms in coastal waters, being exposed to varying levels of solar UV radiation (UVR) and reduced levels of carbon dioxide (CO2). While reduced CO2 availability is known to enhance CO2 concentrating mechanisms (CCMs) in this diatom and others, little is known on the effects of UV on microalgal CCMs, especially when CO2 levels fluctuate in coastal waters. Here, we show that S. costatum upregulated its CCMs in response to UVR (295-395 nm), especially to UVA (320-395 nm) in the presence and absence of photosynthetically active radiation (PAR). The intensity rise of UVA and/or UVR alone resulted in an increase of the activity of extracellular carbonic anhydrase (CAe); and the addition of UVA enhanced the activity of CCMs-related CAe by 23-27% when PAR levels were low. Such UV-stimulated CCMs activity was only significant at the reduced CO2 level (3.4 µmol L-1). In addition, UVA alone drove active HCO3 - uptake although it was not as obvious as CAe activity, another evidence for its role in enhancing CCMs activity. In parallel, the addition of UVA enhanced photosynthetic carbon fixation only at the lower CO2 level compared to PAR alone. In the absence of PAR, carbon fixation increased linearly with increased intensities of UVA or UVR regardless of the CO2 levels. These findings imply that during S. costatum blooming period when CO2 and PAR availability becomes lower, solar UVR (mainly UVA) helps to upregulate its CCMs and thus carbon fixation, enabling its success of frequent algal blooms.

Photosynthesis and calcification of the coccolithophore Emiliania huxleyi are more sensitive to changed levels of light and CO2 under nutrient limitation.

Photophysiological responses of phytoplankton to changing multiple environmental drivers are essential in understanding and predicting ecological consequences of ocean climate changes. In this study, we investigated the combined effects of two CO2 levels (410 and 925 µatm) and five light intensities (80 to 480 µmol photons m-2 s-1) on cellular pigments contents, photosynthesis and calcification of the coccolithophore Emiliania huxleyi grown under nutrient replete and limited conditions, respectively. Our results showed that high light intensity, high CO2 level and nitrate limitation acted synergistically to reduce cellular chlorophyll a and carotenoid contents. Nitrate limitation predominantly enhanced calcification rate; phosphate limitation predominantly reduced photosynthetic carbon fixation rate, with larger extent of the reduction under higher levels of CO2 and light. Reduced availability of both nitrate and phosphate under the elevated CO2 concentration decreased saturating light levels for the cells to achieve the maximal relative electron transport rate (rETRmax). Light-saturating levels for rETRmax were lower than that for photosynthetic and calcification rates under the nutrient limitation. Regardless of the culture conditions, rETR under growth light levels correlated linearly and positively with measured photosynthetic and calcification rates. Our findings imply that E. huxleyi cells acclimated to macro-nutrient limitation and elevated CO2 concentration decreased their light requirement to achieve the maximal electron transport, photosynthetic and calcification rates, indicating a photophysiological strategy to cope with CO2 rise/pH drop in shoaled upper mixing layer above the thermocline where the microalgal cells are exposed to increased levels of light and decreased levels of nutrients.