Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms

Minimum energy (as photon) costs are predicted for core reactions of photosynthesis, for photorespiratory metabolism in algae lacking CO₂ concentrating mechanisms (CCMs) and for various types of CCMs; in algae, with CCMs; allowance was made for leakage of CO₂ from the internal pool. These predicted values are just compatible with the minimum measured photon costs of photosynthesis in microalgae and macroalgae lacking or expressing CCMs. More energy-expensive photorespiration, for example for organisms using Rubiscos with lower CO₂–O₂ selectivity coefficients, would be less readily accommodated within the lowest measured photon costs of photosynthesis by algae lacking CCMs. The same applies to the cases of CCMs with higher energy costs of active transport of protons or inorganic carbon species, or greater allowance for significant leakage from the accumulated intracellular pool of CO₂. High energetic efficiency can involve a higher concentration of catalyst to achieve a given rate of reaction, adding to the resource costs of growth. There are no obvious mechanistic interpretations of the occurrence of CCMs algae adapted to low light and low temperatures using the rationales adopted for the occurrence of C₄ photosynthesis in terrestrial flowering plants. There is an exception for cyanobacteria with low-selectivity Form IA or IB Rubiscos, and those dinoflagellates with low-selectivity Form II Rubiscos, for which very few natural environments have high enough CO₂:O₂ ratios to allow photosynthesis in the absence of CCMs.     

The role of external carbonic anhydrase in photosynthesis during growth of the marine diatom Chaetoceros muelleri

Carbon dioxide concentrating mechanisms (CCMs) act to improve the supply of CO₂ at the active site of ribulose‐1,5‐bisphosphate carboxylase/oxygenase. There is substantial evidence that in some microalgal species CCMs involve an external carbonic anhydrase (CA_ext) and that CA_ext activity is induced by low CO₂ concentrations in the growth medium. However, much of this work has been conducted on cells adapted to air‐equilibrium concentrations of CO₂, rather than to changing CO₂ conditions caused by growing microalgal populations. We investigated the role of CA_ext in inorganic carbon (C_i) acquisition and photosynthesis at three sampling points during the growth cycle of the cosmopolitan marine diatom Chaetoceros muelleri. We observed that CA_ext activity increased with decreasing C_i, particularly CO₂, concentration, supporting the idea that CA_ext is modulated by external CO₂ concentration. Additionally, we found that the contribution of CA_ext activity to carbon acquisition for photosynthesis varies over time, increasing between the first and second sampling points before decreasing at the last sampling point, where external pH was high. Lastly, decreases in maximum quantum yield of photosystem II (F_v/F_m), chlorophyll, maximum relative electron transport rate, light harvesting efficiency (α) and maximum rates of C_i‐ saturated photosynthesis (V_max) were observed over time. Despite this decrease in photosynthetic capacity an up‐regulation of CCM activity, indicated by a decreasing half‐saturation constant for CO₂ (K_0.5CO₂), occurred over time. The flexibility of the CCM during the course of growth in C. muelleri may contribute to the reported dominance and persistence of this species in phytoplankton blooms.     

Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity

We studied the growth and photosynthetic characteristics of a toxic (CS506) and a nontoxic strain (CS509) of the bloom‐forming cyanobacterium Cylindrospermopsis raciborskii grown under identical experimental conditions. When exposed to light‐saturating growth conditions (100 μmol photons · m^?2 · s^?1), values for maximal photosynthetic capacity (P_max) and maximum quantum yield (F_v/F_m) indicated that both strains had an equal ability to process captured photons and deliver them to PSII reaction centers. However, CS506 grew faster than CS509. This was consistent with its higher light requirement for saturation of photosynthesis (I_k). Greater shade tolerance of CS509 was indicated by its higher ability to harvest light (α), lower photosynthetic light compensation point (I_c), and higher chlorophyll a to biovolume ratio. Strain‐specific differences were found in relation to non‐photochemical quenching, effective absorption cross‐sectional area of PSIIα‐centers (σPSIIα), and the antenna connectivity parameter of PSIIα (J_conPSIIα). These findings highlighted differences in the transfer of excitation from phycobilisome/PSII to PSI, on the dependence on different pigments for light harvesting and on the functioning of the PSII reaction centers between the two strains. The results of this study showed that both performance and composition of the photosynthetic apparatus are different between these strains, though with only two strains examined we cannot attribute the performance of strain 506 to its ability to produce cylindrospermopsins. The emphasis on a strain‐specific light adaptation/acclimation is crucial to our understanding of how different light conditions (both quantity and quality) can trigger the occurrence of different C. raciborskii strains and control their competition and/or dominance in natural ecosystems.     

Effect of elevated temperature on the physiological responses of marine <Emphasis Type="Italic">Chlorella</Emphasis> strains from different latitudes

The increased frequency of heat waves due to climate change poses a threat to all organisms. Microalgae are the basis of aquatic food webs, and high temperatures have significant impacts on their adaptation and survival rates. Algae respond to environmental changes by modulating their photosynthetic rates and biochemical composition. This study aims to examine the effect of elevated temperature on similar taxa of marine Chlorella originating from different latitudes. Strains from the Antarctic, temperate zone, and the tropics were grown at various temperatures, ranging from 4 to 38, 18 to 38, and 28 to 40 °C, respectively. A pulse-amplitude modulated (PAM) fluorometer was used to assess their photosynthetic responses. Parameters including maximum quantum efficiency (F _v/F _m), relative electron transport rate (rETR), and light harvesting efficiency (α) were determined from the rapid light curves (RLCs). In addition, the composition of fatty acids was compared to evaluate changes induced by the temperature treatments. Increasing the temperature from 35 to 38 °C for both Antarctic and temperate strains and from 38 to 40 °C for the tropical strain resulted in severe inhibition of photosynthesis and suppressed growth. Although all the strains demonstrated the ability to recover from different stress levels, the tropical strain was able to recover most rapidly while the Antarctic strain had the slowest recovery. The results underline that the thermal threshold for the analysed Chlorella strains temperature ranges between 38 and 40 °C. Furthermore, the analysed strains exhibited different trends in their response to elevated temperatures and recovery capabilities.     

Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

Oxygenic photosynthesis evolved at least 2.4 Ga; all oxygenic organisms use the ribulose bisphosphate carboxylase-oxygenase (Rubisco)-photosynthetic carbon reduction cycle (PCRC) rather than one of the five other known pathways of autotrophic CO(2) assimilation. The high CO(2) and (initially) O(2)-free conditions permitted the use of a Rubisco with a high maximum specific reaction rate. As CO(2) decreased and O(2) increased, Rubisco oxygenase activity increased and 2-phosphoglycolate was produced, with the evolution of pathways recycling this inhibitory product to sugar phosphates. Changed atmospheric composition also selected for Rubiscos with higher CO(2) affinity and CO(2)/O(2) selectivity correlated with decreased CO(2)-saturated catalytic capacity and/or for CO(2)-concentrating mechanisms (CCMs). These changes increase the energy, nitrogen, phosphorus, iron, zinc and manganese cost of producing and operating Rubisco-PCRC, while biosphere oxygenation decreased the availability of nitrogen, phosphorus and iron. The majority of algae today have CCMs; the timing of their origins is unclear. If CCMs evolved in a low-CO(2) episode followed by one or more lengthy high-CO(2) episodes, CCM retention could involve a combination of environmental factors known to favour CCM retention in extant organisms that also occur in a warmer high-CO(2) ocean. More investigations, including studies of genetic adaptation, are needed.     

Inorganic carbon uptake by an Antarctic sea-ice diatom,Nitzschia frigida

There have been no studies to date on the mechanisms of inorganic carbon acquisition by Antarctic microalgae. Consequently, we have examined inorganic carbon (DIC) use inNitzschia frigida, a diatom typical of the Antarctic bottom-ice community. The K_0.5(CO₂) of photosynthesis in this organism was estimated to be 1.09 μM at pH 7.5. The internal concentration of DIC was approximately 4050 μM at an external [DIC] of 45 μM. At air-equilibration levels of inorganic carbon this would be sufficient for a ten-fold accumulation ratio of CO₂. Cells ofN. frigida are capable of carbon-dependent photosynthesis at rates that exceed that expected from uncatalysed CO₂ supply to the cell. About 25% of the total carbonic anhydrase activity appears to be associated with the cell surface inN. frigida. These results support the hypothesis thatN. frigida, like many microalgae from temperate waters, has an active carbon-concentrating mechanism, associated with the ability to utilize external HCO ₃ ⁻ for photosynthesis.     

INTERACTIONS BETWEEN UV‐B EXPOSURE AND PHOSPHORUS NUTRITION. II. EFFECTS ON RATES OF DAMAGE AND REPAIR1

The interactive effects of P starvation and exposure to UV radiation (UVR) on rates of damage ( k ) and repair ( r ), modeled from exposure response curves (ERCs), in the chlorophyte microalga Dunaliella tertiolecta Butcher were investigated. When nutrient‐replete cells were exposed to the UVR during growth, k and r both increased by approximately 62% and 100%, respectively. However, when cells were starved of phosphorus, k increased by a similar amount as observed in replete cells, but r decreased by about 70%, explaining the increased susceptibility of cells to UVR‐induced inhibition of photosynthesis under P starvation. Although not specifically investigated in this study, it is argued that the decreased repair capacity under P starvation is due to a decline in nucleotides such as ATP and GTP, which are necessary for protein repair.     

RAPID AMMONIUM‐ AND NITRATE‐INDUCED PERTURBATIONS TO CHL a FLUORESCENCE IN NITROGEN‐STRESSED DUNALIELLA TERTIOLECTA (CHLOROPHYTA)1

When NH₄ ⁺ or NO₃ ^? was supplied to NO₃ ^? ‐stressed cells of the microalga Dunaliella tertiolecta Butcher, immediate transient changes in chl a fluorescence were observed over several minutes that were not seen in N‐replete cells. These changes were predominantly due to nonphotochemical fluorescence quenching. Fluorescence changes were accompanied by changes in photosynthetic oxygen evolution, indicating interactions between photosynthesis and N assimilation. The magnitude of the fluorescence change showed a Michaelis‐Menten relationship with half‐saturation concentration of 0.5 μM for NO₃ ^? and 10 μM for NH₄ ⁺ . Changes in fluorescence responses were characterized in D. tertiolecta both over 5 days of N starvation and in cells cultured at a range of NO₃ ^? ‐limited growth rates. Variation in responses was more marked in starved than in limited cells. During N starvation, the timing and onset of the fluorescence responses were different for NO₃ ^? versus NH₄ ⁺ and were correlated with changes in maximum N uptake rate during N starvation. In severely N‐starved cells, the major fluorescence response to NO₃ ^? disappeared, whereas the response to NH₄ ⁺ persisted. N‐starved cells previously grown with NH₄ ⁺ alone showed fluorescence responses with NH₄ ⁺ but not NO₃ ^? additions. The distinct responses to NO₃ ^? and NH₄ ⁺ may be due to the differences between regulation of the uptake mechanisms for the two N sources during N starvation. This method offers potential for assessing the importance of NO₃ ^? or NH₄ ⁺ as an N source to phytoplankton populations and as a diagnostic tool for N limitation.     

Environmental influences on akinete germination and development in Nodularia spumigena (Cyanobacteriaceae), isolated from the Gippsland Lakes, Victoria, Australia

This study was carried out to investigate the genesis of N. spumigena blooms by specifically studying the effects of environmental variables (salinity, nitrogen, phosphorus and light) on the germination of N. spumigena akinetes. Optimal conditions for maximum germination and germling growth were determined by exposing akinetes to a range of salinities and nutrient (nitrogen and phosphorus) concentrations under two different irradiances. At pre-determined time periods, treatments were sampled and the percent germination and length of germlings assessed. The results indicated that akinete germination and germling growth were optimal at salinities from 5 to 25 and significantly reduced outside this range. A positive correlation in germination was observed with increasing nutrient (phosphorus and nitrate) concentration. Similarly, germling growth increased with increasing concentrations of both nutrients. Irradiance significantly influenced both germination and growth during salinity experiments, whereas in nutrient addition experiments, irradiance had no effect on germination; however, growth was significantly influenced during phosphorus addition experiments. Consequently, salinity and light appeared to be most critical in the germination process for N. spumigena akinetes, with phosphorus most important for germling growth. The study showed that N. spumigena may be able to germinate under environmental conditions outside its optimal range, but the growth of the germling is significantly reduced, which in turn suggests that its ability to form a bloom outside its optimal environmental conditions would also be greatly reduced.     

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change

Carbon dioxide concentrating mechanisms (also known as inorganic carbon concentrating mechanisms; both abbreviated as CCMs) presumably evolved under conditions of low CO(2) availability. However, the timing of their origin is unclear since there are no sound estimates from molecular clocks, and even if there were, there are no proxies for the functioning of CCMs. Accordingly, we cannot use previous episodes of high CO(2) (e.g. the Palaeocene-Eocene Thermal Maximum) to indicate how organisms with CCMs responded. Present and predicted environmental change in terms of increased CO(2) and temperature are leading to increased CO(2) and HCO(3)(-) and decreased CO(3)(2-) and pH in surface seawater, as well as decreasing the depth of the upper mixed layer and increasing the degree of isolation of this layer with respect to nutrient flux from deeper waters. The outcome of these forcing factors is to increase the availability of inorganic carbon, photosynthetic active radiation (PAR) and ultraviolet B radiation (UVB) to aquatic photolithotrophs and to decrease the supply of the nutrients (combined) nitrogen and phosphorus and of any non-aeolian iron. The influence of these variations on CCM expression has been examined to varying degrees as acclimation by extant organisms. Increased PAR increases CCM expression in terms of CO(2) affinity, whilst increased UVB has a range of effects in the organisms examined; little relevant information is available on increased temperature. Decreased combined nitrogen supply generally increases CO(2) affinity, decreased iron availability increases CO(2) affinity, and decreased phosphorus supply has varying effects on the organisms examined. There are few data sets showing interactions amongst the observed changes, and even less information on genetic (adaptation) changes in response to the forcing factors. In freshwaters, changes in phytoplankton species composition may alter with environmental change with consequences for frequency of species with or without CCMs. The information available permits less predictive power as to the effect of the forcing factors on CCM expression than for their overall effects on growth. CCMs are currently not part of models as to how global environmental change has altered, and is likely to further alter, algal and aquatic plant primary productivity.