Carbon acquisition in relation to CO 2 supply was investigated in three marine bloom-forming microalgae, the diatom Skeletonema costatum, the flagellate Phaeocystis globosa, and the coccolithophorid Emiliania huxleyi. In vivo activities of extracellular (eCA) and intracellular (iCA) carbonic anhydrase activity, photosynthetic O 2 evolution, CO 2 and HCO uptake rates were measured by membrane inlet mass spectrometry in cells acclimated to pCO 2 Ϫ 3 levels of 36, 180, 360, and 1,800 ppmv. Large differences were obtained between species both with regard to the efficiency and regulation of carbon acquisition. While eCA activity increased with decreasing CO 2 concentration in S. costatum and P. globosa, consistently low values were obtained for E. huxleyi. No clear trends with pCO 2 were observed in iCA activity for any of the species tested. Half saturation concentrations (K 1/2 ) for photosynthetic O 2 evolution, which were highest for E. huxleyi and lowest for S. costatum, generally decreased with decreasing CO 2 concentration. In contrast, K 1/2 values for P. globosa remained unaffected by pCO 2 of the incubation. CO 2 and HCO were taken up simultaneously by all species. The relative contribution of HCO to total carbon uptakegenerally increased with decreasing CO 2 , yet strongly differed between species. Whereas K 1/2 for CO 2 and HCO Ϫ 3 uptake was lowest at the lowest pCO 2 for S. costatum and E. huxleyi, it did not change as a function of pCO 2 in P. globosa. The observed taxon-specific differences in CO 2 sensitivity, if representative for the natural environment, suggest that changes in CO 2 availability may influence phytoplankton species succession and distribution. By modifying the relative contribution of different functional groups, e.g., diatomaceous versus calcareous phytoplankton, to the overall primary production this could potentially affect marine biogeochemical cycling and air-sea gas exchange.Marine phytoplankton account for approximately 50% of global primary production (Falkowski et al. 1998). Changes in the oceanic primary production over geological timescales have influenced biogeochemical cycles and thus atmospheric pCO 2 levels. Of the approximately 20,000 phytoplankton species (Falkowski and Raven 1997), however, only a relatively small number of key species control the cycling of carbon and other bioelements. Among these, bloom-forming phytoplankton play a major role in determining vertical fluxes of particulate material. With respect to their specific effects on biogeochemical cycling, phytoplankton can be separated into so-called functional groups (Falkowski et al. 1998), such as silicifying and calcifying phytoplankton, flagellates, and N 2 -fixating cyanobacteria. The relative contribution of each of these groups to marine primary production largely determines biogeochemical cycling in the ocean and the interplay between the various bioelements. What determines the distribution and succession of phytoplankton in space and time, especially with respect to the different func-1...
Rates of cellular uptake of CO 2 and HCO 3 Ϫ during steady-state photosynthesis were measured in the marine diatoms Thalassiosira weissflogii and Phaeodactylum tricornutum, acclimated to CO 2 partial pressures of 36, 180, 360, and 1,800 ppmv. In addition, in vivo activity of extracellular (eCA) and intracellular (iCA) carbonic anhydrase was determined in relation to CO 2 availability. Both species responded to diminishing CO 2 supply with an increase in eCA and iCA activity. In P. tricornutum, eCA activity was close to the detection limit at higher CO 2 concentrations. Simultaneous uptake of CO 2 and HCO 3 Ϫ was observed in both diatoms. At air-equilibrated CO 2 levels (360 ppmv), T. weissflogii took up CO 2 and HCO 3Ϫ at approximately the same rate, whereas CO 2 uptake exceeded HCO 3 Ϫ uptake by a factor of two in P. tricornutum. In both diatoms, CO 2 : HCO 3 Ϫ uptake ratios progressively decreased with decreasing CO 2 concentration, whereas substrate affinities of CO 2 and HCO 3 Ϫ uptake increased. Half-saturation concentrations were always Յ5 M CO 2 for CO 2 uptake and Ͻ700 M HCO 3 Ϫ for HCO 3 Ϫ uptake. Our results indicate the presence of highly efficient uptake systems for CO 2 and HCO 3 Ϫ in both diatoms at concentrations typically encountered in ocean surface waters and the ability to adjust uptake rates to a wide range of inorganic carbon supply.Primary production by marine phytoplankton takes place in an environment that is characterized by high and relatively constant HCO 3 Ϫ concentrations (ϳ2 mM) but low and variable concentrations of molecular dissolved CO 2 [CO 2,aq ] (ϳ5-25 M). Variation in [CO 2,aq ] of ocean surface waters is mainly caused by intense photosynthesis during phytoplankton blooms, differences in water temperature, or mixing with deep water of different CO 2 content. On longer timescales, rising CO 2 concentrations in the upper layers of the ocean are expected in response to the present increase in atmospheric CO 2 partial pressure (pCO 2 ; Houghton et al. 1996). Because these changes in [CO 2,aq ] are always accompanied by changes in pH, concentrations of HCO 3 Ϫ vary much less because of concomitant shifts in the relative proportions of the inorganic carbon (C i ) species.The response of phytoplankton growth to changes in CO 2 supply is largely determined by the mechanism of C i uptake. Several studies indicate that both CO 2 and HCO 3 Ϫ in the bulk seawater are utilized by marine eukaryotic microalgae (e.g., Colman and Rotatore 1995;Rotatore et al. 1995;Korb et al.
Cyanobacteria (blue-green algae) possess an environmental adaptation for survival at low CO2 concentrations. The adaptation is known as a CO2 concentrating mechanism (CCM), and it functions to actively transport and accumulate inorganic carbon ( and CO2; Ci) within the cell and then uses this Ci pool to provide elevated CO2 concentrations around the primary CO2-fixing enzyme, ribulose bisphosphate carboxylase-oxygenase (Rubisco). It appears that the site of CO2 elevation is within a unique microcompartment known as the carboxysome, which is a proteinaceous polyhedral body that contains most, if not all, of the Rubisco within the cell. This review covers comparative aspects of physiology, genetics, and proteins involved in the cyanobacterial CCM with particular focus on recent advances. This review highlights information on three strains of unicellular cyanobacteria, namely Synechocystis PCC6803 (freshwater strain; for which a full genome database is now available), Synechococcus PCC7002 (coastal marine strain) and Synechococcus PCC7942 (freshwater strain). Genes that may be involved in the CCM, directly or indirectly, are summarized in tabular form. For Synechocystis PCC6803, the number of genes related to CCM activity is now in excess of 50; however, 19 of these components have the potential to code for several distinct type-1, NADH dehydrogenase complexes.Key words: cyanobacteria, CO2 concentrating mechanism, carboxysomes, genes, photosynthesis, transporters.
We investigated carbon acquisition by the N 2 -fixing cyanobacterium Trichodesmium IMS101 in response to CO 2 levels of 15.1, 37.5, and 101.3 Pa (equivalent to 150, 370, and 1000 ppm). In these acclimations, growth rates as well as cellular C and N contents were measured. In vivo activities of carbonic anhydrase (CA), photosynthetic O 2 evolution, and CO 2 and HCO { 3 fluxes were measured using membrane inlet mass spectrometry and the 14 C disequilibrium technique. While no differences in growth rates were observed, elevated CO 2 levels caused higher C and N quotas and stimulated photosynthesis and N 2 fixation. Minimal extracellular CA (eCA) activity was observed, indicating a minor role in carbon acquisition. Rates of CO 2 uptake were small relative to total inorganic carbon (Ci) fixation, whereas HCO { 3 contributed more than 90% and varied only slightly over the light period and between CO 2 treatments. The low eCA activity and preference for HCO { 3 were verified by the 14 C disequilibrium technique. Regarding apparent affinities, half-saturation concentrations (K 1/2 ) for photosynthetic O 2 evolution and HCO { 3 uptake changed markedly over the day and with CO 2 concentration. Leakage (CO 2 efflux : Ci uptake) showed pronounced diurnal changes. Our findings do not support a direct CO 2 effect on the carboxylation efficiency of ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) but point to a shift in resource allocation among photosynthesis, carbon acquisition, and N 2 fixation under elevated CO 2 levels. The observed increase in photosynthesis and N 2 fixation could have potential biogeochemical implications, as it may stimulate productivity in N-limited oligotrophic regions and thus provide a negative feedback on rising atmospheric CO 2 levels.
Mass spectrometric measurements of dissolved free 13CO2 were used to monitor CO2 uptake by air grown (low CO2) cells and protoplasts from the green alga Chlamydomonas reinhardtli. In the presence of 50 micromolar dissolved inorganic carbon and light, protoplasts which had been washed free of extemal carbonic anhydrase reduced the 13CO2 concentration in the medium to close to zero. Similar resuits were obtained with low CO2 cells treated with 50 micromolar acetazolamide. Addition of carbonic anhydrase to protoplasts after the period of rapid CO2 uptake revealed that the removal of CO2 from the medium in the light was due to selective and active CO2 transport rather than uptake of total dissolved inorganic carbon. demonstrated for these organisms (2, 4, 9, 15). In the case of cyanobacteria, both HCO3-and CO2 are substrates for active transport (2,3,6,7,14,15) with CO2 being selectively and preferentially used by the cells (2,6,16). In Chlamydomonas, HC03-is actively transported (4, 25, 29), but CO2 uptake has been considered to be passive (18,20). Carbon dioxide, however, is taken up from the medium faster than HCO3-by Chlamydomonas (13,28,29) and several authors (13,29) have considered the possibility of active CO2 transport.Studies on the DIC transport mechanism of green algae are complicated by their cellular compartmentation. Recently, it was shown that isolated chloroplasts of low C02 Chlamydomonas reinhardtii were able to accumulate DIC (19) and a model was presented where the only active DIC transport mechanism was located on the chloroplast envelope (18,19). In that model the plasma membrane was suggested to be only a diffusion barrier for CO2 generated by external carbonic anhydrase. In contrast, by comparison of the apparent affinities for DIC of whole cells and purified chloroplasts, Suiltemeyer et al. (26) came to the conclusion that active transport by the chloroplast alone may not be responsible for the photosynthetic characteristics of whole cells.Another difficulty in examining the DIC species taken up by whole cells is the presence of an external carbonic anhydrase (10) which catalyzes the rapid equilibrium between CO2 and HCO3-, thus making a direct discrimination between CO2 and HCO3-uptake impossible (7, 13). However, using inhibitors for external carbonic anhydrase or the cell-wall less mutant CW-15, some authors came to the conclusion that CO2 and not HCO3-(13) or that both C02 and HCO3- (29) were actively transported.Confusion about which DIC species is actively taken up from the medium may also be caused by methods which only measure total rates of transport rather than transport of CO2 or HC03-individually. Using MS, which measures free dissolved gases in liquid, several authors presented direct eviGreen algae and cyanobacteria possess a high apparent affinity for DIC3 when grown at low DIC concentrations (low CO2 cells: 2,5,9,17), and DIC accumulation has been '
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