How Do Algae Concentrate CO2 to Increase the Efficiency of Photosynthetic Carbon Fixation?1

Abstract

The ability of photosynthetic organisms to use CO 2 for photosynthesis depends in part on the properties of Rubisco. Rubisco has a surprisingly poor affinity for CO 2 , probably because it evolved in an atmosphere that had very high CO 2 levels compared with the present atmosphere. In C 3 plants the K m (CO 2 ) of Rubisco ranges between 15 and 25 m. In cyanobacteria Rubisco has an even lower affinity for CO 2 , and the K m (CO 2 ) can be greater than 200 m. In comparison, the concentration of CO 2 in water in equilibrium with air is approximately 10 m. From these numbers it becomes apparent that Rubisco is operating at no more than 30% of its capacity under standard atmospheric conditions. This is one of the reasons that C 3 plants contain such large amounts of Rubisco. Exacerbating this situation is the fact that O 2 is a competitive substrate with respect to CO 2 .In the atmosphere, where the O 2 level is 21% and the CO 2 level is 0.035%, the competition by O 2 accounts for as much as 30% of the reactions catalyzed by Rubisco. A number of photosynthetic organisms have developed ways to increase the level of CO 2 at the location of Rubisco in the plant. This results in an increase in CO 2 fixation and a decrease in the deleterious oxygenation reaction. An excellent example of a CO 2 -concentrating mechanism in higher plants is C 4 photosynthesis, which has arisen independently in a number of plant families. Aquatic photosynthetic organisms such as the microalgae have also adapted to low CO 2 levels by concentrating CO 2 internally. This Update will focus on CO 2 -concentrating mechanisms in the microalgae. For more detailed reviews of the CO 2 concentration by algae, the reader is referred to the special issue of the Canadian Journal of Botany (1998, Vol. 76) and the article by Raven (1997). TYPES OF CO 2 -CONCENTRATING MECHANISMS AND THE PROBLEM OF LEAKAGE OF ACCUMULATED CO 2C 4 plants are the best-studied organisms that concentrate CO 2 to enhance the carboxylation reaction of Rubisco. They have high levels of PEP carboxylase in leaf mesophyll cells, whereas Rubisco is located primarily in the bundle-sheath cells. CA within the mesophyll converts CO 2 entering the leaf into HCO 3 Ϫ , which is the substrate for PEP carboxylase. The advantages that PEP carboxylase has over Rubisco are its high affinity for HCO 3 Ϫ and its insensitivity to O 2 . At physiological CO 2 levels and pH, the HCO 3 Ϫ concentration in the cytoplasm of mesophyll cells is about 50 m, whereas the K m (HCO 3 Ϫ ) of PEP carboxylase is estimated to be about 8 m. Therefore, in contrast to Rubisco, PEP carboxylase is saturated for HCO 3 Ϫ at ambient CO 2 levels. To finish the CO 2 -concentrating effect of C 4 metabolism, the C 4 acid generated in the mesophyll cells is then transported to the bundle-sheath cells and decarboxylated, creating an elevated CO 2 level specifically within these cells.The problem faced by all photosynthetic organisms that concentrate CO 2 is that it can easily diffuse through biological membranes. How can such a slipp...

The Cia5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas reinhardtii

“…4, lanes 3, 7, 11 and 15 vs. lanes 1, 5, 9 and 13, respectively). As expected from the earlier results of others (4,5,14), no transcripts from any of the CO 2 -responsive genes were detectable in RNA extracted from the cia5 mutant grown under either high or low CO 2 conditions (Fig. 4, lanes 2, 6, 10, and 14).…”

“…For most algae a carbon concentrating mechanism (CCM) is essential for photosynthesis (2)(3)(4)(5). This mechanism enables algae to accumulate intracellular concentrations of CO 2 and HCO 3 Ϫ that are much in excess of the CO 2 and HCO 3 Ϫ concentrations in their often inorganic carbon (C i )-deprived aqueous environments.…”

Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO 2

“…The growth defect of the RNAi lines provides further evidence that Rh1 is a gas channel for CO 2 . At high CO 2 , the CCM is not induced (36,(39)(40)(41)(42)(43)(44) and there is no need to prevent CO 2 regenerated near Rubisco from leaking away. (It is CO 2 , rather than HCO 3 Ϫ , which is the substrate for this enzyme, but probably HCO 3 Ϫ that is accumulated and transferred to the chloroplast by cells grown in air).…”

“…Chlamydomonas genes are highly expressed during growth in air, a circumstance under which the so-called CCM is activated (36,(39)(40)(41)(42)(43)(44). These include genes coding for a periplasmic carbonic anhydrase Cah1 (36,38), the mitochondrial carbonic anhydrase mtCA (32,45), and the chloroplast envelope protein LIP-36 (33,46).…”

Extra and intracelular activities of carbonic anhydrase of the marine microalga Tetraselmis gracilis (Chlorophyta)

“…Internally, CA may be located in the cytoplasm, mitochondria and mainly in the chloroplast (1). In the cytoplasm, the internal enzyme acts converting CO2 into HCO3 -to prevent the leaking of CO2 from the cell (21,22). In the chloroplast HCO3 -is converted to CO2 by another CA, concentrating CO2 around RUBISCO, helping to overcome the low affinity that this enzyme has for CO2 (5) and thus, being part of the Carbon Concentrating Mechanism that is found mainly in microalgae and cyanobacteria (7,16,22).…”