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

How Do Algae Concentrate CO2 to Increase the Efficiency of Photosynthetic Carbon Fixation
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  Update on Photosynthesis How Do Algae Concentrate CO 2 to Increase the Efficiency of Photosynthetic Carbon Fixation? 1 James V. Moroney* and Aravind Somanchi Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 The ability of photosynthetic organisms to use CO 2 forphotosynthesis 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 hadvery high CO 2 levels compared with the present atmo-sphere. In C 3 plants the K  m (CO 2 ) of Rubisco ranges be-tween 15 and 25 ␮ m . In cyanobacteria Rubisco has an evenlower affinity for CO 2 , and the K  m (CO 2 ) can be greater than200 ␮ m . In comparison, the concentration of CO 2 in waterin equilibrium with air is approximately 10 ␮ m . From thesenumbers it becomes apparent that Rubisco is operating atno more than 30% of its capacity under standard atmo-spheric conditions. This is one of the reasons that C 3 plantscontain such large amounts of Rubisco. Exacerbating thissituation is the fact that O 2 is a competitive substrate withrespect 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 muchas 30% of the reactions catalyzed by Rubisco. A number of photosynthetic organisms have developed ways to increasethe level of CO 2 at the location of Rubisco in the plant. Thisresults in an increase in CO 2 fixation and a decrease in thedeleterious oxygenation reaction. An excellent example of a CO 2 -concentrating mechanism in higher plants is C 4 pho-tosynthesis, which has arisen independently in a number of plant families. Aquatic photosynthetic organisms such asthe microalgae have also adapted to low CO 2 levels byconcentrating CO 2 internally. This Update will focus onCO 2 -concentrating mechanisms in the microalgae. Formore 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 ANDTHE PROBLEM OF LEAKAGE OF ACCUMULATED CO 2 C 4 plants are the best-studied organisms that concentrateCO 2 to enhance the carboxylation reaction of Rubisco. Theyhave high levels of PEP carboxylase in leaf mesophyll cells,whereas Rubisco is located primarily in the bundle-sheathcells. CA within the mesophyll converts CO 2 entering theleaf into HCO 3 Ϫ , which is the substrate for PEP carboxy-lase. The advantages that PEP carboxylase has overRubisco are its high affinity for HCO 3 Ϫ and its insensitivityto O 2 . At physiological CO 2 levels and pH, the HCO 3 Ϫ concentration in the cytoplasm of mesophyll cells is about50 ␮ m , whereas the K  m (HCO 3 Ϫ ) of PEP carboxylase isestimated to be about 8 ␮ m . Therefore, in contrast toRubisco, PEP carboxylase is saturated for HCO 3 Ϫ at ambi-ent CO 2 levels. To finish the CO 2 -concentrating effect of C 4 metabolism, the C 4 acid generated in the mesophyll cells isthen transported to the bundle-sheath cells and decarboxy-lated, creating an elevated CO 2 level specifically withinthese cells.The problem faced by all photosynthetic organisms thatconcentrate CO 2 is that it can easily diffuse through bio-logical membranes. How can such a slippery substance beaccumulated? In C 4 plants CO 2 is concentrated in specific bundle-sheath cells within the leaf. These are the only cellscontaining significant amounts of Rubisco. Here the thick-ened cell walls of the bundle sheath prevent the diffusionof the CO 2 generated by decarboxylation reactions. Mi-croalgae face an additional problem in that they are com-posed of only one or a few cells, all with ready access to theenvironment; therefore, they must prevent the diffusion of CO 2 out of the cell while allowing the entry of othernutrients.Microalgae overcome the problem of CO 2 diffusion byaccumulating HCO 3 Ϫ . Being a charged species, HCO 3 Ϫ diffuses through membranes much more slowly than CO 2 .However, because CO 2 is the substrate required byRubisco, the accumulated HCO 3 Ϫ must be converted toCO 2 before C i fixation takes place. This appears to beaccomplished by packaging Rubisco within the algal celland generating the CO 2 at that location through the actionof a CA. A locally elevated CO 2 environment is therebycreated in which CO 2 can out-compete O 2 at the active siteof Rubisco. This allows the CO 2 to be used for photosyn-thesis before it can diffuse out of the cell. Thus, microalgaethat concentrate CO 2 package Rubisco in a very specificlocation, have a means of concentrating HCO 3 Ϫ , and havea means of converting the accumulated HCO 3 Ϫ to CO 2 rapidly at the location of Rubisco. 1 This work was supported by National Science Foundationgrant no. IBN-9632087.* Corresponding author; e-mail; fax1–504–388–8459.Abbreviations: ABC, ATP-binding cassette; CA, carbonic anhy-drase; C i , inorganic carbon. Plant Physiology  , January 1999, Vol. 119, pp. 9–16, © 1999 American Society of Plant Physiologists9  THE LOCATION OF RUBISCO IN MICROALGAE In higher plants Rubisco appears to act largely as asoluble protein that is distributed throughout the chloro-plast stroma. By analogy, one might expect eukaryoticalgae to have Rubisco throughout their chloroplast stromaand cyanobacteria to contain Rubisco throughout their cy-toplasm, but this is clearly not the case. In most microalgaeRubisco is concentrated in a specific location: in carboxy-somes in cyanobacteria and in the pyrenoid in algae (Fig. 1;Table I). Recent studies support the hypothesis thatRubisco localization is required for efficient acquisition of environmental CO 2 .Carboxysomes are electron-dense particles that are sur-rounded by a protein shell. Evidence that they containlarge amounts of Rubisco is extensive. In fact, isolatedcarboxysomes have been found to be composed mostly of Rubisco (Price et al., 1992). Immunolocalization studiesusing antibodies raised against Rubisco indicate that thecarboxysome is the primary location in cyanobacteria(McKay et al., 1993). A mutation that causes a 30-aminoacid extension of the Rubisco small subunit leads to aRubisco that does not pack into the carboxysome, whichleaves the carboxysome empty (Schwarz et al., 1995). Mu-tations in any of the genes affecting the assembly, function-ing, or shape of the carboxysome result in cells that cannotgrow on air levels of CO 2 (Price et al., 1998).Rubisco is also packaged in microalgae, where it is themajor protein component of the pyrenoid. Pyrenoids have been purified from both Eremosphera (Okada, 1992) and Chlamydomonas reinhardtii (Kuchitsu et al., 1991), and in both cases they consisted primarily of Rubisco. In addition, C. reinhardtii cells with a mutation of the rbcL gene (Rubiscolarge subunit) that leads to a truncation of the large subunitof Rubisco have no pyrenoids (Rawat et al., 1996). Al-though it is accepted that Rubisco is the major constituentof the pyrenoid, there are conflicting findings regardingwhat percentage of the cell’s Rubisco is in the pyrenoid. Arecent report by Borkhsenious et al. (1998) demonstratedthat in C. reinhardtii the amount of Rubisco in the stromavaries with growth conditions.In all published immunolocalization studies the pyre-noid is densely labeled when an anti-Rubisco antibody isused as the primary probe (Borkhsenious et al., 1998). Anexample of this immunogold labeling is shown in Figure1D. In these studies the amount of Rubisco in each subcel-lular location was estimated by multiplying the density of particles (particles per area) in that location by the averagevolume of the pyrenoid (2.4 mm 3 ) or the stroma (35.6 mm 3 )(Lacoste-Royal and Gibbs, 1987). However, this still leavesa fairly broad range of estimates for the amount of Rubiscoin the pyrenoid, from 50% to 99%. These differences could be attributed to the growth regime used by the various Figure 1. Carboxysomes and pyrenoids in dif-ferent photosynthetic organisms. A, Electron mi-crograph of the cyanobacteria Anabaena ; B,electron micrograph of the green alga C. rein- hardtii  ; C, electron micrograph of the diatom Amphora ; D, Immunogold labeling of the pyre-noid of  C. reinhardtii  with an anti-Rubisco anti-body. Bars ϭ 0.5 ␮ m. Cs, Carboxysome; Py,pyrenoid. 10 Moroney and Somanchi Plant Physiol. Vol. 119, 1999  research groups. Borkhsenious et al. (1998) found that theamount of Rubisco in the stroma varied with growth con-ditions: about 50% of the Rubisco was localized to thepyrenoid in C. reinhardtii cells grown on elevated CO 2 (5%,v/v). In contrast, they reported that when C. reinhardtii cells were grown under low CO 2 (ambient levels of CO 2 areconsidered low) more than 90% of the Rubisco was locatedin the pyrenoid. These results are consistent with those of Morita et al. (1997), who reported that 99% of the Rubiscowas located in the pyrenoid in cells grown with ambientlevels of CO 2 . C. reinhardtii concentrates CO 2 only when it is grownunder low-CO 2 conditions. Because more than 90% of theRubisco is localized to the pyrenoid under low-CO 2 condi-tions, one question is whether pyrenoidal Rubisco is activein CO 2 fixation or whether the pyrenoid is a storage body.In vitro measurements of Rubisco activity imply that theenzyme in the pyrenoid must be active to account for thelevels of CO 2 fixation observed in C. reinhardtii . A specificlocalization of Rubisco to the pyrenoid is also compatiblewith the view that organisms that have CO 2 -concentratingmechanisms specifically package Rubisco. In lichens and bryophytes there is a good correlation between the opera-tion of a CO 2 -concentrating mechanism and the presence of a pyrenoid (Smith and Griffiths, 1996). In cyanobacteria itappears that the CO 2 level is elevated within the carboxy-some (Price et al., 1998), thus favoring carboxylation activ-ity over the oxygenation activity of Rubisco. The pyrenoidmay serve a similar function in C. reinhardtii and othermicroalgae. THE ACCUMULATION OF HCO 3 The physiological evidence for the existence of CO 2 con-centration in microalgae is 2-fold. First, algae are veryefficient at pulling C i out of the environment. They aremuch more efficient than would be expected, with cellsshowing an apparent affinity for CO 2 of about 1 ␮ m versusthe K  m (CO 2 ) of Rubisco of about 20 ␮ m . In some cases thegrowth conditions of the alga influences the cell’s affinityfor CO 2 . Some species of algae, when grown on elevatedCO 2 concentrations (10 times higher than ambient), are notefficient in their acquisition of C i (Matsuda et al., 1998).However, if these same algae are grown on limiting CO 2 they become very efficient in CO 2 uptake and fixation. Thisimplies that there are inducible transport mechanisms, be-cause the amount of Rubisco does not change during ad-aptation from high- to low-CO 2 conditions.Second, the accumulation of C i within the cell can bemeasured directly. In the light, cyanobacteria can concen-trate HCO 3 Ϫ within the cell more than 100-fold (Miller etal., 1990). Eukaryotic algae are not as efficient but canaccumulate HCO 3 Ϫ at least 20-fold over ambient CO 2 lev-els. C i transporters and CAs may enable the cells to accu-mulate HCO 3 Ϫ within the cell. The exact identity of the C i transporters is still unknown, but recent work has identi-fied some transporters that may play a significant role inthe accumulation of C i (Okamura et al., 1997).In cyanobacteria difficulty in obtaining CO 2 - andHCO 3 Ϫ -transport mutants has been proposed to indicatethe presence of multiple transporters for CO 2 and HCO 3 Ϫ .There is physiological evidence for three types of transport-ers: (a) a Na ϩ -independent HCO 3 Ϫ transporter, (b) a Na ϩ -dependent HCO 3 Ϫ transporter, and (c) a CO 2 transporter.Na ϩ -independent HCO 3 Ϫ transport under extreme C i limitation (Espie and Kandasamy, 1992) and a difference inthe magnitude of the requirement of Na ϩ for HCO 3 Ϫ trans-port versus CO 2 transport (Miller et al., 1990) have beendetected in Synechococcus PCC 7942. These data indicate thepresence of either a Na ϩ /HCO 3 Ϫ symporter (Espie andKandasamy, 1994) or the regulation of pH throughNa ϩ /H ϩ antiport mechanisms.A mutant of  Synechococcus PCC 7942, M42, has beenshown to have a reduced affinity for HCO 3 Ϫ . The mutationin M42 has been shown to be in the gene cluster cmpABCD ,which codes for a Na ϩ -independent, high-affinity HCO 3 Ϫ transporter induced under low C i (Okamura et al., 1997).This is the first reported primary transporter for HCO 3 Ϫ ,and belongs to the subfamily of ABC transporters alsoknown as traffic ATPases (Higgins, 1992). The presence of an ABC-type transporter indicates that at high pH, whenHCO 3 Ϫ is taken up, ATP may be the energy source for C i uptake. A high-CO 2 -requiring mutant of  Synechococcus PCC 7942 has recently been characterized; it has a lesion inthe gene dc14 (Ronen-Tarazi et al., 1998), which encodes aputative Na ϩ -dependent HCO 3 Ϫ transporter. This trans-porter may be responsible for the fast induction response tolow CO 2 reported from Synechococcus PCC 7942 and Syn-echocystis PCC 7002 (Su¨ltemeyer et al., 1997).Much less is known about the transport of C i in microal-gae. Extracellular C i has to pass through at least two mem- brane systems to reach the site of carboxylation, whichmakes transport more complex than in cyanobacteria. Atleast two types of C i uptake can be observed in microalgae.There is evidence for both direct transport of HCO 3 Ϫ andCA-facilitated diffusion of CO 2 across the membrane. Thetwo membranes that we will consider as possible sites of C i transport are the plasma membrane and the chloroplastenvelope. Table I. Location of Rubisco in organisms with different types of photosynthesis  Photosynthesis TypeAbility toConcentrate CO 2 ?Rubisco Location C 3 photosynthesis (higher plants) No Chloroplast stroma of most cells in leaf C 4 photosynthesis (higher plants) Yes Chloroplast stroma of bundle-sheath cellsEukaryotic microalgae Yes Pyrenoid of the chloroplastCyanobacteria Yes Carboxysomes CO 2 Concentration by Microalgae 11  At the plasma membrane there is evidence for bothHCO 3 Ϫ uptake and CA-facilitated diffusion. In Scenedesmusobliquus there is very good evidence that HCO 3 Ϫ is takenup directly by the cell (Thielmann et al., 1990). These cellscan photosynthesize even when the pH is greater than 10and HCO 3 Ϫ and CO 32 Ϫ are the major C i species. Chlorellasaccharophila also appears to take up HCO 3 Ϫ , although CO 2 is its preferred C i source (Williams et al., 1995).The other major process by which microalgae take up C i is through the uptake of CO 2 . Many microalgae producelarge amounts of CA when grown on limiting CO 2 (Raven,1997). CA is a zinc metalloprotein, often located in theperiplasmic space of the cell, that catalyzes the intercon-version of CO 2 and HCO 3 Ϫ according to the followingformula:CO 2 ϩ H 2 O 7 H 2 CO 3 7 H ϩ ϩ HCO 3 Ϫ Genes encoding periplasmic CAs have been identified in both Dunaliella salina and C. reinhardtii (Fujiwara et al.,1990). CA1, the periplasmic CA, has been identified as oneof the prominent low-CO 2 -inducible proteins in C. rein-hardtii . The ability of microalgal cells to use externalHCO 3 Ϫ for photosynthesis has been correlated with thepresence of periplasmic CA. The presence of external CAinhibitors decreased the use of external C i for photosyn-thesis (Moroney et al., 1985). The periplasmic CA probablyincreases the efficiency with which the cells can take inexternal C i . This includes both the supply of CO 2 fordiffusion across the plasma membrane and the supply of HCO 3 Ϫ for the plasma membrane’s HCO 3 Ϫ -transportsystem.The chloroplast envelope is another possible location of HCO 3 Ϫ accumulation (Beardall, 1981). Intact chloroplastsisolated from C. reinhardtii and Dunaliella tertiolecta retainthe ability to accumulate HCO 3 Ϫ when grown on low CO 2 ,and have the ability to concentrate CO 2 . At low CO 2 , C.reinhardtii induces the synthesis of LIP-36, a transport pro-tein that is localized to the chloroplast envelope (Chen etal., 1997). LIP-36 belongs to a family of transport proteinsthat often act as exchangers (e.g. ATP for ADP transport-ers). It is possible that LIP-36 plays a role in HCO 3 Ϫ accu-mulation by the chloroplast, because chloroplasts withLIP-36 accumulate HCO 3 Ϫ and those without LIP-36, iso-lated from high-CO 2 -grown cells, do not. The fact thatLIP-36 is encoded by two separate genes (Chen et al., 1997)has made it difficult to obtain mutants devoid of thisprotein. THE GENERATION OF CO 2 AT THELOCATION OF RUBISCO The generation of CO 2 at the location of Rubisco isaccomplished through the action of a CA located at or nearRubisco. In cyanobacteria a CA is localized to the carboxy-some (Price et al., 1992). Carboxysomes purified from Syn-echocystis species have significant CA activity. In Synecho-cystis 6803, for which the complete genome has beensequenced, only one CA gene has been identified. The roleof this CA is the dehydration of accumulated HCO 3 Ϫ toform a localized, elevated concentration of CO 2 in thecarboxysome. Loss of the carboxysomal CA through mu-tation leads to a cell that cannot grow well on limitinglevels of CO 2 (Fukuzawa et al., 1992). In addition, cellsmissing the carboxysomal CA actually accumulate HCO 3 Ϫ to higher levels than wild-type cells, presumably becausethe cell can no longer convert the HCO 3 Ϫ to CO 2 forphotosynthesis. In these CA-deficient cells, the CO 2 -concentrating mechanism is still operational, but the finalconversion of HCO 3 Ϫ to CO 2 is too slow.It is noteworthy that CA activity is not found in thecytoplasm of cyanobacteria. Price and Badger (1989) dem-onstrated that transforming Synechococcus species with ahuman CA actually “short-circuits” HCO 3 Ϫ accumulation,and this transformant requires high CO 2 for growth. Thehuman CA was localized to the cytoplasm and convertedthe accumulated HCO 3 Ϫ to CO 2 . The CO 2 thus formed thenleaked from the cell and could not be used efficiently forphotosynthesis. From these studies it appears that the lo-cation of the internal CA is as important as the packagingof Rubisco.In eukaryotic algae CA is often found inside the cell andin the periplasmic space. It is now clear that C. reinhardtii has at least five genes that encode CAs. Two of these genes, Cah1 and Cah2 , encode CAs that are directed to theperiplasmic space (Fujiwara et al., 1990). Two more genesencode mitochondrial CAs (Eriksson et al., 1996). Recently,a fifth gene, Cah3 , was found to encode a chloroplast CA(Karlsson et al., 1998). This CA has a leader sequence thatdirects the protein into the lumen of the thylakoid mem- brane. Pharmacological and genetic evidence indicates thatCah3 is essential in generating an elevated CO 2 concentra-tion for Rubisco. It appears to play a role similar to that of the carboxysomal CA of cyanobacteria. This thylakoid CAis sensitive to sulfonamides, pharmaceuticals often used toinhibit mammalian CAs. Treatment of  C. reinhardtii withsulfonamides that can enter the cell results in repression of CO 2 fixation (Moroney et al., 1985). Sulfonamides alsoseverely inhibit photosynthesis in many other algae at lowCO 2 concentrations, indicating that this thylakoid CA may be found in many algae. Furthermore, mutant strains of Cah3 are unable to grow at low CO 2 , although the ability of these strains to accumulate HCO 3 Ϫ is not impaired. Thethylakoid CA is thought to increase the concentration of CO 2 in the chloroplast by dehydration of the high concen-tration of HCO 3 Ϫ the cell accumulates there.Chloroplast CAs from higher plants are quite differentfrom the Cah3 protein of  C. reinhardtii. Cah3 does not shareany sequence similarity with higher-plant chloroplast CAs.The higher-plant enzymes are of the ␤ -type and are foundin the chloroplast stroma (Badger and Price, 1994). In con-trast, Cah3 is of the ␣ -type and is found in the thylakoidlumen (Karlsson et al., 1998). At this point no stromal CAhas been found in an algal species that actively concen-trates CO 2 . It appears that a stromal CA might short-circuitthe active accumulation of HCO 3 Ϫ . If CA were present inthe chloroplast stroma it might convert accumulatedHCO 3 Ϫ  back to CO 2 , allowing it to leak out of the cell before being fixed by Rubisco. 12 Moroney and Somanchi Plant Physiol. Vol. 119, 1999  A MODEL FOR CO 2 CONCENTRATION Even though the types of cells that possess CO 2 -concentrating abilities are very different, they have certainproperties in common that allow them to use CO 2 effi-ciently. The first property is the ability to accumulateHCO 3 Ϫ in some fashion. For most cyanobacteria and manyeukaryotic algae, HCO 3 Ϫ can be transported into the celldirectly. For other eukaryotic algae, particularly those thatlive in acidic environments, where the concentration of HCO 3 Ϫ is low, CO 2 is the C i species that enters the cell andHCO 3 Ϫ is accumulated in the chloroplast. A second prop-erty is that Rubisco is usually packaged in a very specificway within the photosynthetic cell. Although it is possiblethat not every microalgal cell that concentrates CO 2 has acarboxysome or a pyrenoid, most cyanobacteria have car- boxysomes and most microalgae have pyrenoids. The thirdproperty that appears to be common among these types of cells is the presence of a CA near the location of Rubisco.The CA supplies the Rubisco with CO 2 from the pool of HCO 3 Ϫ . Loss of this CA through mutation or inhibitiongreatly impairs the cell’s ability to use external C i forphotosynthesis (Price et al., 1992; Karlsson et al., 1998).A general model for CO 2 concentration in cyanobacteriais shown in Figure 2. Evidence for this model comes fromphysiological experiments and mutant analysis (Table II).In Figure 2 three different types of transporters are shownat the plasma membrane. It is very likely that there are anumber of transporters important in HCO 3 Ϫ accumulation, because no single mutation has totally inhibited it. Recentwork with the Cmp gene cluster of cyanobacteria hasshown that high-affinity HCO 3 Ϫ -transporter activity is lostif genes within this operon are deleted (Okamura et al.,1997). The Cmp operon appears to encode an ABC trans-porter with significant similarity to proteins known totransport small anions such as NO 3 Ϫ (Ogawa et al., 1998;Ohkawa et al., 1998). The fact that Cmp deletion mutantsstill retain the ability to grow on low HCO 3 Ϫ concentra-tions implies that other transporters remain to be identi-fied. This is consistent with the multiple transport activitiesdetected in the physiological experiments.The amount of energy required for HCO 3 Ϫ uptake is notclear at present. Because ABC transporters require ATP, itis reasonable to assume that some ATP is used in HCO 3 Ϫ uptake (Fig. 2). Ogawa et al. (1998) have provided supportfor this contention by identifying a number of mutationsthat encode subunits of a NAD(P)H dehydrogenase. Dele-tions of these ndh genes lead to cells that require high CO 2 for photoautotrophic growth. The explanation for thesemutants is that cyclic electron transport is disrupted inthese cells such that too little ATP is made to supportHCO 3 Ϫ transport. Mi et al. (1992) have also provided evi-dence that cyclic electron transport around PSI is requiredfor HCO 3 Ϫ uptake.Because Rubisco uses CO 2 and not HCO 3 Ϫ , the HCO 3 Ϫ accumulated by the cyanobacteria must be converted toCO 2 for fixation. As indicated in Table II, any disruption of the proper localization of Rubisco to the carboxysome incyanobacteria leads to a cell that requires high CO 2 forphotoautotrophic growth. One example of this is the loss of carboxysomes through loss of the carboxysomal shell pro-teins (Oru´s et al., 1995), in which case Rubisco is distrib-uted in the cytoplasm. A similar situation occurs in themutant EK6, which contains a 30-amino acid extension of the small subunit of Rubisco and has empty carboxysomes(Schwarz et al., 1995). Even though the kinetics of this Figure 2. A model for CO 2 concentration in cyanobacteria. The fontsizes of CO 2 and HCO 3 Ϫ indicate the relative concentrations of theseC i species. PGA, 3-Phosphoglyceric acid. Table II. High-CO  2 -requiring strains and constructs of cyanobacteria Strain or Construct Mutant Phenotype Process Disrupted Explanation M3 and D4 a Lack of carboxysomes Rubisco packaging Carboxysomes fail to form; Rubisco islocated in cytoplasmStrain with Rhodospirillum rubrum  Rubisco b Rubisco in cytoplasm Rubisco packaging Bacterial Rubisco does not locate tocarboxysomeExtension of Rubisco smallsubunit c Empty carboxysomes Rubisco packaging Rubisco cannot package into carboxysomeCmp deletions d ABC transporter lost HCO 3 Ϫ accumulation High-affinity HCO 3 Ϫ transport lostHCA II transformant e CA in cytoplasm HCO 3 Ϫ accumulation Accumulated HCO 3 Ϫ leaks out as CO 2 IcfA deletion f  Loss of carboxysome CA CO 2 generation HCO 3 Ϫ not converted to CO 2 incarboxysomeNumerous ndh deletions g Loss of NADH dehydrogenase Energy mutations Cyclic electron flow is disrupted a Oru´s et al. (1995). b Pierce et al. (1989). c Schwarz et al. (1995). d Okamura et al. (1997); Price et al. (1998). e Price andBadger (1989). f  Fukuzawa et al. (1992). g Ogawa et al. (1998); Price et al. (1998). CO 2 Concentration by Microalgae 13
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