Photophysiological responses of Southern Ocean phytoplankton to changes in CO2 concentrations: Short-term versus acclimation effects

The present study examines how different pCO2 acclimations affect the CO2- and light-dependence of photophysiological processes and O2 fluxes in four Southern Ocean (SO) key phytoplankton species. We grew Chaetoceros debilis (Cleve), Pseudo-nitzschia subcurvata (Hasle), Fragilariopsis kerguelensis (O'Meara) and Phaeocystis antarctica (Karsten) under low (160 µatm) and high (1000 ?atm) pCO2. The CO2- and light-dependence of fluorescence parameters of photosystem II (PSII) were determined by means of a fluorescence induction relaxation system (FIRe). In all tested species, nonphotochemical quenching (NPQ) is the primary photoprotection strategy in response to short-term exposure to high light or low CO2 concentrations. In C. debilis and P. subcurvata, PSII connectivity (p) and functional absorption cross-sections of PSII in ambient light (sigma PSII') also contributed to photoprotection while changes in re-oxidation times of Qa acceptor (tQa) were more significant in F. kerguelensis. The latter was also the only species being responsive to high acclimation pCO2, as these cells had enhanced relative electron transport rates (rETRs) and sigma PSII' while tQa and p were reduced under short-term exposure to high irradiance. Low CO2-acclimated cells of F. kerguelensis and all pCO2 acclimations of C. debilis and P. subcurvata showed dynamic photoinhibition with increasing irradiance. To test for the role and presence of the Mehler reaction in C. debilis and P. subcurvata, the light-dependence of O2 fluxes was estimated using membrane inlet mass spectrometry (MIMS). Our results show that the Mehler reaction is absent in both species under the tested conditions. We also observed that dark respiration was strongly reduced under high pCO2 in C. debilis while it remained unaltered in P. subcurvata. Our study revealed species-specific differences in the photophysiological responses to pCO2, both on the acclimation as well as the short-term level.

Seawater carbonate chemistry and combined mechanistic effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101, 2010

The marine diazotrophic cyanobacterium Trichodesmium responds to elevated atmospheric CO2 partial pressure (pCO2) with higher N2 fixation and growth rates. To unveil the underlying mechanisms, we examined the combined influence of pCO2(150 and 900 µatm) and light (50 and 200 µmol photons m-2 s-1) on TrichodesmiumIMS101. We expand on a complementary study that demonstrated that while elevated pCO2 enhanced N2 fixation and growth, oxygen evolution and carbon fixation increased mainly as a response to high light. Here, we investigated changes in the photosynthetic fluorescence parameters of photosystem II, in ratios of the photosynthetic units (photosystem I:photosystem II), and in the pool sizes of key proteins involved in the fixation of carbon and nitrogen as well as their subsequent assimilation. We show that the combined elevation in pCO2 and light controlled the operation of the CO2-concentrating mechanism and enhanced protein activity without increasing their pool size. Moreover, elevated pCO2 and high light decreased the amounts of several key proteins (NifH, PsbA, and PsaC), while amounts of AtpB and RbcL did not significantly change. Reduced investment in protein biosynthesis, without notably changing photosynthetic fluxes, could free up energy that can be reallocated to increase N2 fixation and growth at elevated pCO2 and light. We suggest that changes in the redox state of the photosynthetic electron transportchain and posttranslational regulation of key proteins mediate the high flexibility in resources and energy allocation in Trichodesmium. This strategy should enableTrichodesmium to flourish in future surface oceans characterized by elevated pCO2, higher temperatures, and high light.

Ocean acidification accelerates reef bioerosion

In the recent discussion how biotic systems may react to ocean acidification caused by the rapid rise in carbon dioxide partial pressure (pCO2) in the marine realm, substantial research is devoted to calcifiers such as stony corals. The antagonistic process-biologically induced carbonate dissolution via bioerosion- has largely been neglected. Unlike skeletal growth, we expect bioerosion by chemical means to be facilitated in a high-CO2 world. This study focuses on one of the most detrimental bioeroders, the sponge Cliona orientalis, which attacks and kills live corals on Australia's Great Barrier Reef. Experimental exposure to lowered and elevated levels of pCO2 confirms a significant enforcement of the sponges' bioerosion capacity with increasing pCO2 under more acidic conditions. Considering the substantial contribution of sponges to carbonate bioerosion, this finding implies that tropical reef ecosystems are facing the combined effects of weakened coral calcification and accelerated bioerosion, resulting in critical pressure on the dynamic balance between biogenic carbonate build-up and degradation.

Effects of ocean acidification and global warming on reef bioerosion-lessons from a clionaid sponge

Coral reefs are under threat, exerted by a number of interacting effects inherent to the present climate change, including ocean acidification and global warming. Bioerosion drives reef degradation by recycling carbonate skeletal material and is an important but understudied factor in this context. Twelve different combinations of pCO2 and temperature were applied to elucidate the consequences of ocean acidification and global warming on the physiological response and bioerosion rates of the zooxanthellate sponge Cliona orientalis-one of the most abundant and effective bioeroders on the Great Barrier Reef, Australia. Our results confirm a significant amplification of the sponges' bioerosion capacity with increasing pCO2, which is expressed by more carbonate being chemically dissolved by etching. The health of the sponges and their photosymbionts was not affected by changes in pCO2, in contrast to temperature, which had significant negative impacts at higher levels. However, we could not conclusively explain the relationship between temperature and bioerosion rates, which were slightly reduced at both colder as well as warmer temperatures than ambient. The present findings on the effects of ocean acidification on chemical bioerosion, however, will have significant implications for predicting future reef carbonate budgets, as sponges often contribute the lion's share of internal bioerosion on coral reefs.

Effects of ocean acidification on Posidonia oceanica epiphytic community and shoot productivity

1. Biological interactions can alter predictions that are based on single-species physiological response. It is known that leaf segments of the seagrass Posidonia oceanica will increase photosynthesis with lowered pH, but it is not clear whether the outcome will be altered when the whole plant and its epiphyte community, with different respiratory and photosynthetic demands, are included. In addition, the effects on the Posidonia epiphyte community have rarely been tested under controlled conditions, at near-future pH levels. 2. In order to better evaluate the effects of pH levels as projected for the upcoming decades on seagrass meadows, shoots of P. oceanica with their associated epiphytes were exposed in the laboratory to three pH levels (ambient: 8.1, 7.7 and 7.3, on the total scale) for 4 weeks. Net productivity, respiration, net calcification and leaf fluorescence were measured on several occasions. At the end of the study, epiphyte community abundance and composition, calcareous mass and crustose coralline algae growth were determined. Finally, photosynthesis vs. irradiance curves (PE) was produced from segments of secondary leaves cleaned of epiphytes and pigments extracted. 3. Posidonia leaf fluorescence and chlorophyll concentrations did not differ between pH treatments. Net productivity of entire shoots and epiphyte-free secondary leaves increased significantly at the lowest pH level yet limited or no stimulation in productivity was observed at the intermediate pH treatment. Under both pH treatments, significant decreases in epiphytic cover were observed, mostly due to the reduction of crustose coralline algae. The loss of the dominant epiphyte producer yet similar photosynthetic response for epiphyte-free secondary leaves and shoots suggests a minimal contribution of epiphytes to shoot productivity under experimental conditions. 4. Synthesis. Observed responses indicate that under future ocean acidification conditions foreseen in the next century an increase in Posidonia productivity is not likely despite the partial loss of epiphytic coralline algae which are competitors for light. A decline in epiphytic cover could, however, reduce the feeding capacity of the meadow for invertebrates. In situ long-term experiments that consider both acidification and warming scenarios are needed to improve ecosystem-level predictions.

Response of spring diatoms to CO2 availability in the Western North Pacific as determined by next-generation sequencing

Next-generation sequencing (NGS) technologies have enabled us to determine phytoplankton community compositions at high resolution. However, few studies have adopted this approach to assess the responses of natural phytoplankton communities to environmental change. Here, we report the impact of different CO2 levels on spring diatoms in the Oyashio region of the western North Pacific as estimated by NGS of the diatom-specific rbcL gene (DNA), which encodes the large subunit of RubisCO. We also examined the abundance and composition of rbcL transcripts (cDNA) in diatoms to assess their physiological responses to changing CO2 levels. A short-term (3-day) incubation experiment was carried out on-deck using surface Oyashio waters under different pCO2 levels (180, 350, 750, and 1000 µatm) in May 2011. During the incubation, the transcript abundance of the diatom-specific rbcL gene decreased with an increase in seawater pCO2 levels. These results suggest that CO2 fixation capacity of diatoms decreased rapidly under elevated CO2 levels. In the high CO2 treatments (750 and 1000 µatm), diversity of diatom-specific rbcL gene and its transcripts decreased relative to the control treatment (350µatm), as well as contributions of Chaetocerataceae, Thalassiosiraceae, and Fragilariaceae to the total population, but the contributions of Bacillariaceae increased. In the low CO2 treatment, contributions of Bacillariaceae also increased together with other eukaryotes. These suggest that changes in CO2 levels can alter the community composition of spring diatoms in the Oyashio region. Overall, the NGS technology provided us a deeper understanding of the response of diatoms to changes in CO2 levels in terms of their community composition, diversity, and photosynthetic physiology.

The impact of fluctuating light on the dinoflagellate Prorocentrum micans depends on NO3- and CO2 availability

Increasing atmospheric pCO2 and its dissolution into oceans leads to ocean acidification and warming, which reduces the thickness of upper mixing layer (UML) and upward nutrient supply from deeper layers. These events may alter the nutritional conditions and the light regime to which primary producers are exposed in the UML. In order to better understand the physiology behind the responses to the concomitant climate changes factors, we examined the impact of light fluctuation on the dinoflagellate Prorocentrum micans grown at low (1 µmol/L) or high (800 µmol/L) [NO3(-)] and at high (1000 µatm) or low (390 µatm, ambient) pCO2. The light regimes to which the algal cells were subjected were (1) constant light at a photon flux density (PFD) of either 100 (C100) or 500 (C500) µmol/m**2/s or (2) fluctuating light between 100 or 500 µmol photons/m**2/s with a frequency of either 15 (F15) or 60 (F60) min. Under continuous light, the initial portion of the light phase required the concomitant presence of high CO2 and NO3(-) concentrations for maximum growth. After exposure to light for 3h, high CO2 exerted a negative effect on growth and effective quantum yield of photosystem II (F'(v)/F'(m)). Fluctuating light ameliorated growth in the first period of illumination. In the second 3h of treatment, higher frequency (F15) of fluctuations afforded high growth rates, whereas the F60 treatment had detrimental consequences, especially when NO3(-) concentration was lower. F'(v)/F'(m) respondent differently from growth to fluctuating light: the fluorescence yield was always lower than at continuous light at 100 µmol/m**2/s, and always higher at 500 µmol/m**2/s. Our data show that the impact of atmospheric pCO2 increase on primary production of dinoflagellate depends on the availability of nitrate and the irradiance (intensity and the frequency of irradiance fluctuations) to which the cells are exposed. The impact of global change on oceanic primary producers would therefore be different in waters with different chemical and physical (mixing) properties.

Physicochemical and photosynthetic characteristics of water samples obtained during a CCGS Amundsen cruise in 2008

During summer 2008, as part of the Circumpolar Flaw Lead system study, we measured phytoplankton photosynthetic parameters to understand regional patterns in primary productivity, including the degree and timescale of photoacclimation and how variability in environmental conditions influences this response. Photosynthesis-irradiance measurements were taken at 15 sites primarily from the depth of the subsurface chlorophyll a (Chl a) maximum (SCM) within the Beaufort Sea flaw lead polynya. The physiological response of phytoplankton to a range of light levels was used to assess maximum rates of carbon (C) fixation (P*m), photosynthetic efficiency (alpha*), photoacclimation (Ek), and photoinhibition (beta*). SCM samples taken along a transect from under ice into open water exhibited a >3-fold increase in alpha* and P*m, showing these parameters can vary substantially over relatively small spatial scales, primarily in response to changes in the ambient light field. Algae were able to maintain relatively high rates of C fixation despite low light at the SCM, particularly in the large (>5 µm) size fraction at open water sites. This may substantially impact biogenic C drawdown if species composition shifts in response to future climate change. Our results suggest that phytoplankton in this region are well acclimated to existing environmental conditions, including sea ice cover, low light, and nutrient pulses. Furthermore, this photoacclimatory response can be rapid and keep pace with a developing SCM, as phytoplankton maintain photosynthetic rates and efficiencies in a narrow ''shade-acclimated'' range.

Surface water properties, phytoplankton composition and photosynthesis rates of Amundsen Sea sites

The phytoplankton community composition and productivity in waters of the Amundsen Sea and surrounding sea ice zone were characterized with respect to iron (Fe) input from melting glaciers. High Fe input from glaciers such as the Pine Island Glacier, and the Dotson and Crosson ice shelves resulted in dense phytoplankton blooms in surface waters of Pine Island Bay, Pine Island Polynya, and Amundsen Polynya. Phytoplankton biomass distribution was the opposite of the distribution of dissolved Fe (DFe), confirming the uptake of glacial DFe in surface waters by phytoplankton. Phytoplankton biomass in the polynyas ranged from 0.6 to 14 µg Chl a / L, with lower biomass at glacier sites where strong upwelling of Modified Circumpolar Deep Water from beneath glacier tongues was observed. Phytoplankton blooms in the polynyas were dominated by the haptophyte Phaeocystis antarctica, whereas the phytoplankton community in the sea ice zone was a mix of P. antarctica and diatoms, resembling the species distribution in the Ross Sea. Water column productivity based on photosynthesis versus irradiance characteristics averaged 3.00 g C /m**2/d in polynya sites, which was approximately twice as high as in the sea ice zone. The highest water column productivity was observed in the Pine Island Polynya, where both thermally and salinity stratified waters resulted in a shallow surface mixed layer with high phytoplankton biomass. In contrast, new production based on NO3 uptake was similar between different polynya sites, where a deeper UML in the weakly, thermally stratified Pine Island Bay resulted in deeper NO3 removal, thereby offsetting the lower productivity at the surface. These are the first in situ observations that confirm satellite observations of high phytoplankton biomass and productivity in the Amundsen Sea. Moreover, the high phytoplankton productivity as a result of glacial input of DFe is the first evidence that melting glaciers have the potential to increase phytoplankton productivity and thereby CO2 uptake, resulting in a small negative feedback to anthropogenic CO2 emissions.

Experiments on polar seaweeds

Organisms populating benthic shallow water systems of both polar regions are adapted to a particularly harsh environment. We studied effects of freezing and the combination of high light intensities and low water temperatures on photosynthesis of key macroalgal species from the Arctic intertidal (Fucus distichus) and Antarctic subtidal (Palmaria decipiens). Photosynthetic activity of F. distichus specimens was monitored during the freezing process; there was a marked decrease in quantum yield with decreasing temperatures, and a rapid recovery as soon as temperatures increased again. Thus, under the experimental conditions tested, no indication of photodamage was found. Specimens of Palmaria were exposed to a combination of high light intensities and low water temperatures. A persistent impairment of photosynthetic activity occurred at 0°C at light intensities of 400 µmol photons m-2 s-1. In all treatments, there was a decreasing ratio of phycobiliproteins to chlorophyll a. Overall, the two studies provide baseline data for interpreting physiological responses of two important macroalgal species in an extreme environment, the polar coastal ecosystem.

Photochemical responses of the diatom Skeletonema costatum grown under elevated CO2 concentrations to short-term changes in pH

Variability in pH is a common occurrence in many aquatic environments, due to physical, chemical and biological processes. In coastal waters, lagoons, estuaries and inland waters, pH can change very rapidly (within seconds or hours) in addition to daily and seasonal changes. At the same time, progressive ocean acidification caused by anthropogenic CO2 emissions is superimposed on these spatial and temporal pH changes. Photosynthetic organisms are therefore unavoidably subject to significant pH variations at the cell surface. Whether this will affect their response to long-term ocean acidification is still unknown, nor is it known whether the short-term sensitivity to pH change is affected by the pCO2 to which the cells are acclimated. We posed the latter open question as our experimental hypothesis: Does acclimation to seawater acidification affect the response of phytoplankton to acute pH variations? The diatom Skeletonema costatum, commonly found in coastal and estuarine waters where short-term acute changes in pH frequently occur, was selected to test the hypothesis. Diatoms were grown at both 390 (pH 8.2, low CO2; LC) and 1000 (pH 7.9, high CO2; HC) µatm CO2 for at least 20 generations, and photosynthetic responses to short-term and acute changes in pH (between 8.2 and 7.6) were investigated. The effective quantum yield of LC-grown cells decreased by ca. 70% only when exposed to pH 7.6; this was not observed when exposed to pH 7.9 or 8.2. HC-grown cells did not show significant responses in any pH treatment. Non-photochemical quenching showed opposite trends. In general, our results indicate that while LC-grown cells are rather sensitive to acidification, HC-grown cells are relatively unresponsive in terms of photochemical performance.