Combined effects of inorganic carbon and light on Phaeocystis globosa Scherffel (Prymnesiophyceae)(update)

Phaeocystis globosa (Prymnesiophyceae) is an ecologically dominating phytoplankton species in many areas around the world. It plays an important role in both the global sulfur and carbon cycles, by the production of dimethylsulfide (DMS) and the drawdown of inorganic carbon. Phaeocystis globosa has a polymorphic life cycle and is considered to be a harmful algal bloom (HAB) forming species. All these aspects make this an interesting species to study the effects of increasing carbon dioxide (CO2) concentrations, due to anthropogenic carbon emissions.

Here, the combined effects of three different dissolved carbon dioxide concentrations (CO2(aq)) (low: 4 μmol kg−1, intermediate: 6–10 μmol kg−1 and high CO2(aq): 21–24 μmol kg−1) and two different light intensities (low light, suboptimal: 80 μmol photons m−2 s−1 and high light, light saturated: 240 μmol photons m−2 s−1) are reported.

The experiments demonstrated that the specific growth rate of P. globosa in the high light cultures decreased with increasing CO2(aq) from 1.4 to 1.1 d−1 in the low and high CO2 cultures, respectively. Concurrently, the photosynthetic efficiency (FV/FM) increased with increasing CO2(aq) from 0.56 to 0.66. The different light conditions affected photosynthetic efficiency and cellular chlorophyll a concentrations, both of which were lower in the high light cultures as compared to the low light cultures. These results suggest that in future inorganic carbon enriched oceans, P. globosa will become less competitive and feedback mechanisms to global change may decrease in strength.

Prolonged exposure to elevated CO2 promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima

Some photosynthetic organisms benefit from elevated levels of carbon dioxide, but studies on the effects of elevated PCO₂ on the algal symbionts of animals are very few. This study investigated the impact of hypercapnia on a photosynthetic symbiosis between the anemone Anthopleura elegantissima and its zooxanthella Symbiodinium muscatinei. Anemones were maintained in the laboratory for 1 week at 37 Pa PCO₂ and pH 8.1. Clonal pairs were then divided into two groups and maintained for 6 weeks under conditions naturally experienced in their intertidal environment, 45 Pa PCO₂, pH 8.1 and 231 Pa PCO₂, pH 7.3. Respiration and photosynthesis were measured after the 1-week acclimation period and after 6 weeks in experimental conditions. Density of zooxanthellal cells, zooxanthellal cell size, mitotic index and chlorophyll content were compared between non-clonemate anemones after the 1-week acclimation period and clonal anemones at the end of the experiment. Anemones thrived in hypercapnia. After 6 weeks, A. elegantissima exhibited higher rates of photosynthesis at 45 Pa (4.2 µmol O₂ g⁻¹ h⁻¹) and 231 Pa (3.30 µmol O₂ g⁻¹ h⁻¹) than at the initial 37 Pa (1.53 µmol O₂ g⁻¹ h⁻¹). Likewise, anemones at 231 Pa received more of their respiratory carbon from zooxanthellae (CZAR  = 78.2%) than those at 37 Pa (CZAR  = 66.6%) but less than anemones at 45 Pa (CZAR  = 137.3%). The mitotic index of zooxanthellae was significantly greater in the hypercapnic anemones than in anemones at lower PCO₂. Excess zooxanthellae were expelled by their hosts, and cell densities, cell diameters and chlorophyll contents were not significantly different between the groups. The response of A. elegantissima to hypercapnic acidification reveals the potential adaptation of an intertidal, photosynthetic symbiosis for high PCO₂.

Reduced calcification decreases photoprotective capability in the coccolithophorid Emiliania huxleyi

Intracellular calcification of coccolithophores generate CO₂ and consumes additional energy for acquisition of calcium and bicarbonate ions, therefore, it may correlate with photoprotective processes by influencing the energetics. To address this hypothesis, a calcifying Emiliania huxleyi strain (CS-369) was grown semi-continuously at reduced (0.1 mM, LCa) and ambient Ca²⁺ concentrations (10 mM, HCa) for 150 days (>200 generations). The HCa-grown cells had higher photosynthetic and calcification rates and higher contents of chl a and carotenoids compared to the naked (bearing no coccoliths) LCa-grown cells. When exposed to stress-full levels of PAR, LCa-grown cells displayed lower photochemical yield and less efficient non-photochemical quenching (NPQ). When the LCa or HCa-grown cells were inversely shifted to their counterpart medium, LCa to HCa transfer increased photosynthetic carbon fixation (P), calcification rate (C), C/P ratio, NPQ and pigments contents, while those shifted from HCa to LCa exhibited the opposite performance. Increased NPQ, carotenoids and quantum yield clearly linked with increased or sustained calcification in E. huxleyi. The calcification must have played a role in dissipating excessive energy or as an additional drainage of electrons absorbed by the photosynthetic antennae. This phenomenon was further supported by testing two noncalcifying strains, which showed insignificant changes photosynthetic carbon fixation and NPQ when transferred to LCa condition.

Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients

Predicting the impacts of ocean acidification on coastal ecosystems requires an understanding of the effects on macroalgae and their grazers, as these underpin the ecology of rocky shores. Whilst calcified coralline algae (Rhodophyta) appear to be especially vulnerable to ocean acidification, there is a lack of information concerning calcified brown algae (Phaeophyta), which are not obligate calcifiers but are still important producers of calcium carbonate and organic matter in shallow coastal waters. Here we compare ecological shifts in sub-tidal rocky shore systems along CO₂ gradients created by volcanic seeps in the Mediterranean and Papua New Guinea, focussing on abundant macroalgae and grazing sea urchins. In both the temperate and tropical systems the abundances of grazing sea urchins declined dramatically along CO₂ gradients. Temperate and tropical species of the calcifying macroalgal genus Padina (Dictyoaceae, Phaeophyta) showed reductions in CaCO₃ content with CO₂ enrichment. In contrast to other studies of calcified macroalgae, however, we observed an increase in the abundance of Padina spp. in acidified conditions. Reduced sea urchin grazing pressure and significant increases in photosynthetic rates may explain the unexpected success of decalcified Padina spp. at elevated levels of CO₂. This is the first study to provide a comparison of ecological changes along CO₂ gradients between temperate and tropical rocky shores. The similarities we found in the responses of Padina spp. and sea urchin abundance at several vent systems increases confidence in predictions of the ecological impacts of ocean acidification over a large geographical range.

Productivity gains do not compensate for reduced calcification under near-future ocean acidification in the photosynthetic benthic foraminifera Marginopora vertebralis

Changes in the seawater carbonate chemistry (ocean acidification) from increasing atmospheric carbon dioxide (CO₂) concentrations negatively affect many marine calcifying organisms, but may benefit primary producers under dissolved inorganic carbon (DIC) limitation. To improve predictions of the ecological effects of ocean acidification, the net gains and losses between the processes of photosynthesis and calcification need to be studied jointly on physiological and population levels. We studied productivity, respiration, and abundances of the symbiont-bearing foraminifera Marginopora vertebralis on natural CO₂ seeps in Papua New Guinea and conducted additional studies on production and calcification on the Great Barrier Reef (GBR) using artificially enhanced pCO₂. Net oxygen production increased up to 90% with increasing pCO₂, with temperature, light and pH together explaining 61% of the variance in production. Production increased with increasing light and increasing pCO₂, and declined at higher temperatures. Respiration was also significantly elevated (~25%), while calcification was reduced (16-39%) at low pH/high pCO₂ compared to present day conditions. In the field, M. vertebralis was absent at three CO₂ seep sites at pH_Total levels below ~7.9 (pCO₂ ~700 μatm), but it was found in densities of over 1000 m⁻² at all three control sites. The study showed that endosymbiotic algae in foraminifera benefit from increased DIC availability, and may be naturally carbon limited. The observed reduction in calcification may have been caused either by increased energy demands for proton pumping (measured as elevated rates of respiration), or by stronger competition for DIC from the more productive symbionts. The net outcome of these two competing processes is that M. vertebralis cannot maintain populations under pCO₂ exceeding 700 μatm, thus are likely to be extinct in the next century.

Major cellular and physiological impacts of ocean acidification on a reef building coral

As atmospheric levels of CO₂ increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO₂ conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.

Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliania huxleyi (Haptophyta)

Increasing anthropogenic carbon dioxide is causing changes to ocean chemistry, which will continue in a predictable manner. Dissolution of additional atmospheric carbon dioxide leads to increased concentrations of dissolved carbon dioxide and bicarbonate and decreased pH in ocean water. The concomitant effects on phytoplankton ecophysiology, leading potentially to changes in community structure, are now a focus of concern. Therefore, we grew the coccolithophore Emiliania huxleyi (Lohmann) W. W. Hay et H. Mohler and the diatom strains Thalassiosira pseudonana (Hust.) Hasle et Heimdal CCMP 1014 and Thalassiosira pseudonana CCMP 1335 under low light in turbidostat photobioreactors bubbled with air containing 390 ppmv or 750 ppmv CO2. Increased pCO2 led to increased growth rates in all three strains. Additionally, protein levels of RUBISCO increased in the coastal strains of both species, showing a larger capacity for CO2 assimilation at 750 ppmv CO2. With increased pCO2, both T. pseudonana strains displayed an increased susceptibility to PSII photoinactivation, and to compensate, an augmented capacity for PSII repair. Consequently the cost of maintaining PSII function for the diatoms increased at increased pCO2. In E. huxleyi, PSII photoinactivation and the counter-acting repair, while both intrinsically larger than in T. pseudonana, did not change between the current and high-pCO2 treatments. The content of the photosynthetic electron transport intermediary Cytb6f complex increased significantly in the diatoms under elevated pCO2, suggesting changes in electron transport function.

Combined effects of inorganic carbon and light on Phaeocystis globosa Scherffel (Prymnesiophyceae)

Phaeocystis globosa (Prymnesiophyceae) is a globally dominating phytoplankton species. It plays an important role in both the global sulfur and carbon cycles, by the production of dimethylsulfide (DMS) and the drawdown of inorganic carbon. Phaeocystis globosa has a polymorphic life cycle and is considered to be a harmful algal bloom (HAB) forming species. All these aspects make this an interesting species to study the effects of increasing carbon dioxide (CO2) concentrations, due to anthropogenic carbon emissions. Here, the combined effects of three different dissolved carbon dioxide concentrations (CO2(aq)) (low: 4 μmol kg−1, intermediate: 6–10 μmol kg−1 and high CO2(aq): 21–24 μmol kg−1) and two different light intensities (low light, suboptimal: 80 μmol photons m−2s–1 and high light, light saturated: 240 μmol photons m−2s−1) are reported. The experiments demonstrated that the specific growth rate of P. globosa in the high light cultures decreased with increasing CO2(aq) from 1.4 to 1.1 d−1 in the low and high CO2 cultures respectively. Concurrently, the photosynthetic efficiency increased with increasing CO2(aq) from 0.56 to 0.66. The different light conditions affected photosynthetic efficiency and chlorophyll-a concentrations, both of which were lower in the high light cultures as compared to the low light cultures. These results suggest that in the future, inorganic carbon enriched oceans, P. globosa will become less competitive and feedback mechanisms to global change may decrease in strength.

The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH

The effect of ocean acidification conditions has been investigated in cultures of the diatom Thalassiosira pseudonana CCMP1335. Expected end-of-the-century pCO2 (aq) concentrations of 760 µatm (equivalent to pH 7.8) were compared with present-day condition (380 µatm CO2, pH 8.1). Batch culture pH changed rapidly because of CO2 (aq) assimilation and pH targets of 7.8 and 8.1 could not be sustained. Long-term (~100 generation) pH-auxostat, continuous cultures could be maintained at target pH when cell density was kept low (<2×105 cells mL−1). After 3 months continuous culture, the C:N ratio was slightly decreased under high CO2 conditions and red fluorescence per cell was slightly increased. However, no change was detected in photosynthetic efficiency (Fv/Fm) or functional cross section of PS II (σPSII). Elevated pCO2 has been predicted to be beneficial to diatoms due to reduced cost of carbon concentration mechanisms. There was reduced transcription of one putative δ-carbonic anhydrase (CA-4) after 3 months growth at increased CO2 but 3 other δ-CAs and the small subunit of RUBISCO showed no change. There was no evidence of adaptation or clade selection of T. pseudonana after ~100 generations at elevated CO2. On the basis of this long-term culture, pH change of this magnitude in the future ocean may have little effect on T. pseudonana in the absence of genetic adaption.

Combined effect of sea surface warming and ocean acidification on coccolithophores at cold seas

Sea surface warming and ocean acidification are known to be the greatest phenomenon affecting the growth and physiology of marine organisms, in particular on calcifiers. Coccolithophores represent an important group of calcifying unicellular algae and play an important role in the global carbon. In this study, the effect of increased pCO2 (186, 384 and 784 ppmV CO2 corresponding to glacial, present and future CO2 conditions respectively) and sea surface warming especially at cold seas (4, 6 and 8°C) at the exponential growth phase of Emiliania huxleyi was examined using a semi continuous batch culture experiments. It has been showed that the growth rate was proportional to the increasing temperature and inversely proportional to the pCO2 increase. The effect of temperature on organic production was highly significant as the Coccosphere size, POC (particulate organic carbon) per cell and PIC (particulate inorganic carbon) per cell was decreased with the increase in temperature. POC per cell increased and PIC per cell decreased with increase in pCO2 resulted in lower PIC: POC ratios at future CO2 concentrations which indicate reduction in export of organic carbon as lower PIC/POC ratio will reduce the ballast effect on the sinking cells at the future pCO2 conditions. The difference in PIC: POC ratios were higher at higher temperatures. C: N ratios were much higher than the Redfield ratios of 6.625 at higher temperatures indicating more carbon sequestration per nitrate input where as no significant impact of pCO2 observed on C: N ratios. Scanning electron micrographs also showed reduction in coccosphere size with increase in temperature and coccolith malformation at the present and future pCO2 conditions. In general, the results show that sea surface warming will favor the E huxleyi cells at nutrient replete conditions to increase growth rate but ocean acidification will have adverse effect on PIC/POC ratios of coccolithophorid cells and the proportion of impact on PIC/POC ration would increase with sea surface warming at cold seas.