Photosynth Res (2007) 93:69–77 DOI 10.1007/s11120-006-9128-y
REVIEW
Cyanobacterial NADPH dehydrogenase complexes Teruo Ogawa Æ Hualing Mi
Received: 22 August 2006 / Accepted: 18 December 2006 / Published online: 6 February 2007 Ó Springer Science+Business Media B.V. 2007
Abstract Cyanobacteria possess functionally distinct multiple NADPH dehydrogenase (NDH-1) complexes that are essential to CO2 uptake, photosystem-1 cyclic electron transport and respiration. The unique nature of cyanobacterial NDH-1 complexes is the presence of subunits involved in CO2 uptake. Other than CO2 uptake, chloroplastic NDH-1 complex has a similar role as cyanobacterial NDH-1 complexes in photosystem-1 cyclic electron transport and respiration (chlororespiration). In this mini-review we focus on the structure and function of cyanobacterial NDH-1 complexes and their phylogeny. The function of chloroplastic NDH-1 complex and characteristics of plants defective in NDH-1 are also described for comparison. Keywords Cyanobacteria Chlororespiration CO2 uptake NAD(P)H dehydrogenase Photosystem-1 cyclic electron transport Respiration Abbreviations NDH-1, NAD(P)H dehydrogenase PQ Plastoqunone PS Photosystem WT Wild type
T. Ogawa (&) H. Mi National Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China e-mail:
[email protected]
Overview Complex I (NDH-1; NADH ubiquinone oxidoreductase) catalyses the first step in the mitochondrial electron transport chain and is composed of at least 43 unlike polypeptides (bovine heart enzyme). On the other hand, complex I of Escherichia coli is composed of 14 subunits, 11 of which were identified in cyanobacteria and in chloroplasts (Friedrich and Scheide 2000). The three subunits (NuoE, NuoF and NuoG) involved in accepting electrons from NADH in E. coli are missing from cyanobacterial and chloroplastic NDH-1. Recently, four new subunits were identified in cyanobacterial NDH-1 (Prommeenate et al. 2004; Zhang et al. 2004; Battchikova et al. 2005) and three of them are found in chloroplastic NDH-1 (Rumeau et al. 2005; Battchikova et al. 2005). In addition, genes in Arabidopsis are suggested to encode new subunits of NDH-1 and their homologues are present in cyanobacterial genomes (Munshi et al. 2005; Tsuyoshi Endo, personal communication). One of them appears to be involved in accepting electrons from NAD(P)H. Reverse genetic and proteomic studies have demonstrated the involvement of cyanobacterial NDH-1 in CO2 uptake (Ogawa 1991a, b, 1992) and the presence of functionally distinct multiple NDH-1 complexes (Ohkawa et al. 2000; Shibata et al. 2001; Maeda et al. 2002; Herranen et al. 2004; Zhang et al. 2004, 2005). We describe in this mini-review the recent development of the studies on the structure and function of cyanobacterial NDH-1 complexes. The role of chloroplastic NDH-1 complex is also described for comparison.
123
70
Genes encoding subunits of NDH-1 Multiple copies of ndhD and ndhF genes The whole genome sequence data base for Synechocystis sp. PCC 6803 (hereafter Synechocystis PCC 6803) has shown the presence of genes for 15 subunits of NDH-1 with the hydrophobic NdhA, NdhB, NdhC, NdhD, NdhE, NdhF, NdhG and NdhL subunits being membrane components and NdhH, NdhI, NdhJ, NdhK and newly found NdhM, NdhN and NdhO being peripheral subunits (Kaneko et al. 1996; http:// www.kazusa.or.jp/cyano/). The sequence data revealed that ndhD and ndhF are present as gene families with four and three members, respectively, named ndhD1, ndhD2, ndhD3, ndhD4, ndhF1, ndhF3 and ndhF4, although most ndh genes are present as single copies. A phylogenetic tree indicated that NdhD and NdhF proteins are both members of a larger family and may be related by an ancient gene duplication event (Shibata et al. 2001). The lineage branched to the ndhD3and ndhD4-types is present only in cyanobacteria. An evolutionary relationship between cyanobacterial ndhD1/ndhD2-type and ndhD genes in chloroplast genomes is noted. The tree also indicated that ndhF1, ndhF3 and ndhF4 propagated from the ndhF line. Whereas the ndhF1 is related to the chloroplast ndhF, the ndhF3/ndhF4-type genes are present only in cyanobacteria. cupA, cupB and cupS genes Reverse genetic studies have demonstrated cupA (chyY) and cupB (chyX) as subunits of NDH-1 complexes involved in CO2 uptake (Shibata et al. 2001; Maeda et al. 2002). Proteomic studies have identified CupA and a small protein (designated CupS) encoded by sll1735 in Synechocystis PCC 6803 and tll0221 in Thermosynechococcus (Zhang et al. 2004, 2005) as subunits of NDH-1 complexes. All the cup genes are confined to cyanobacteria (Shibata et al. 2001). Newly identified subunits Two D-gel analyses of NDH-1 complexes of Synechocystis PCC 6803 identified three new peripheral subunits named NdhM, NdhN and NdhO (Prommeenate et. al. 2004; Zhang et al. 2004; Battchikova et al. 2005). The homologues of all these subunits were found in chloroplasts of higher plants (Rumeau et al. 2005). Since these chloroplast genes were identified independently, they were named in the order different from those in Synechocystis PCC 6803. Namely, NdhM,
123
Photosynth Res (2007) 93:69–77
NdhN and NdhO in Synechocystis PCC 6803 were named as NdhN, NdhO and NdhM in higher plants, respectively. Unification of the gene (protein) names is required. Analysis of a high CO2-requiring (HCR) mutant of Synechocystis PCC 6803, RKb, indicated that a gene encoding a membrane protein consisting of 80 amino acids is a subunit of NDH-1 and was named as ndhL (renamed from ictA) (Ogawa 1991b, 1992). The gene product (NdhL) was recently identified in NDH-1 complex of Synechocystis PCC 6803 (Battchikova et al. 2005). Genes homologous to ndhL are present in the genomes of rice and Arabidopsis but the homology is not high and the protein is not yet identified in chloroplasts. Analysis of Arabidopsis mutants defective in NDH1 indicated that a gene crr7 might encode a new peripheral subunit of chloroplastic NDH-1 and homologous genes are present in cyanobacterial genomes (Munshi et al. 2005). The gene product has not yet been identified in cyanobacteria. An Arabidopsis gene, crr6, is involved in subunit assembly and stabilization of chloroplastic NDH-1. The homologues of this gene are present in cyanobacterial genomes (Munshi et al. 2006). Recently, new genes encoding subunits of chloroplastic NDH-1 have also been identified in Arabidopsis nuclear genomes. One of these genes encodes a protein containing [2Fe-2S] motif that could function to accept electrons from NAD(P)H (Tsuyoshi Endo, personal communication). Homologues of this gene are present in cyanobacterial genomes.
Low CO2-induced expression of ndh and cup genes Table 1 summarizes ratio changes in transcript abundance of various ndh and cup genes 200 min after downshift of CO2 availability in Synechocystis PCC 6803, calculated from the microarray data (Wang et al. 2004). Expression of ndhF3-ndhD3-cupA operon and cupS is strongly induced under low CO2, whereas expression of the ndhF4-ndhD4 operon, cupB, ndhD1 and ndhF1 genes is suppressed or not affected by low CO2 (Ohkawa et al. 1998; Shibata et al. 2001). The transcript levels of other ndh genes also increased under low CO2. A transcription factor, ndhR, has been identified to regulate the expression of the ndhF3-ndhD3-cupA operon, which was expressed constitutively even under high CO2 conditions when ndhR was inactivated (Figge et al. 2001). The sbtA gene that encodes an HCO-3 transporter and is expressed under low CO2 (Shibata et al. 2002a) is also constitutively expressed under high CO2 in the DndhR mutant (Wang et al. 2004).
Photosynth Res (2007) 93:69–77
71
Table 1 Ratio changes in transcript abundance of various ndh and cup genes 200 min after downshift of CO2 availability in Synechocystis PCC 6803, calculated from the microarray data (Wang et al. 2004) Genes
Ratios
Genes
Ratios
Genes
Ratios
Genes
Ratios
NdhA NdhB NdhC ndhD1 ndhD2 ndhD3
4.3 5.3 5.2 0.6 3.9 35.2
ndhD4 ndhE ndhF1 ndhF3 ndhF4 ndhG
1.0 2.0 0.9 56.9 1.1 2.5
ndhH ndhI ndhJ ndhK ndhL ndhM
2.3 3.5 4.0 4.0 1.3 1.7
ndhN ndhO cupA cupB cupS
2.0 1.1 28.4 0.6 8.9
Expression of ndh genes is also induced by high light intensity. The transcript level of ndhD2, ndhD3 and ndhF3 increased 8–11 times 15 min after exposure of cells to high light intensity whereas high light intensity had little effect on the expression of ndhD1, ndhD4 and ndhF4 (Hihara et al. 2001). The gene product of ndhB was also increased under strong light but decreased in the dark (Mi et al. 2001). The activity and amount of NDH-1 complexes are strongly affected by low CO2 (Zhang et al. 2004; Deng et al. 2003a, b) and also by the growth phase of cells (Ma and Mi 2005). The activity of light-dependent NADPH oxidation was much higher in cells grown under low CO2 than in those grown under high CO2 and was highest in cells at a logarithmic phase of the growth.
Multiple functions of NDH-1 complexes CO2 uptake Cyanobacteria utilize both CO2 and HCO-3 as carbon species (Volokita et al. 1984). Two CO2-uptake systems and three HCO-3 transporters have been identified in Synechocystis PCC 6803 and other cyanobacterial strains (Shibata et al. 2001, 2002a; Maeda et al. 2002; Omata et al. 1999; Price et al. 2004). The isolation of Synechocystis PCC 6803 mutants (RKa and RKb) defective in CO2 uptake and identification of ndhB and ndhL impaired in the mutants was the first demonstration of the essential role of NDH-1 in CO2 uptake (Ogawa 1990, 1991a, b, 1992). The mutants, M55 and M9, were constructed by inserting a kanamycin-resistance cassette to ndhB and ndhL, respectively, and have been analyzed extensively for their physiological characteristics. Although the mechanism of CO2 uptake is not yet known, it is postulated that CO2 enters the cells by diffusion and is converted to HCO-3 on NDH-1 complexes (Kaplan and Reinhold 1999; Tchernov et al. 2001) localized on thylakoid membrane (Ohkawa et al. 2001; Zhang et al. 2004).
Physiological studies of single and double mutants constructed by inactivating the four different ndhD genes led to the finding of functionally distinct NDH-1 complexes (Ohkawa et al. 1998; Klughammer et al. 1999; Ohkawa et al. 2000; Shibata et al. 2001; Maeda et al. 2002). A double mutant where ndhD3 and ndhD4 were inactivated did not take up CO2 and was unable to grow under low CO2 (Ohkawa et al. 2000; Shibata et al. 2001). These ndhD genes constitute operons of ndhF3-ndhD3-cupA and ndhF4-ndhD4 in Synechocystis PCC 6803 and an operon of ndhF4-ndhD4-cupB is found in many other strains. The expression of the ndhF3-ndhD3-cupA is induced under low CO2, whereas the ndhF4-ndhD4 operon and cupB are constitutively expressed. Double mutants, where two genes, one from each operon, were inactivated, did not take up CO2 (Shibata et al. 2002b). This led to the finding of two CO2-uptake systems, one dependent on ndhD3 ndhF3 and cupA and the other dependent on ndhD4 ndhF4 and cupB. The CO2-uptake system dependent on ndhD3/ndhF3/cupA shows high affinity to CO2 and is induced under low CO2, whereas the system dependent on ndhD4/ndhF4/cupB shows low affinity to CO2 and is constitutively expressed (Shibata et al. 2001). CupS is also a constituent of the high affinity system (Zhang et al. 2004). However, inactivation of the gene (sll1735) in Synechocystis PCC 6803 did not show the phenotype as observed with DndhD3 mutant (Ohkawa et al. 1998). Photosystem1-dependent cyclic electron transport The primary evidence for NDH-1-dependent cyclic electron flow was obtained from analysis of redox kinetics of P700 in Synechococcus sp. PCC 7002 (Mi et al. 1992a). Only 10% of P700 was oxidized by weak far-red light (>720 nm, 3 Wm–2) in this cyanobacterium. The low level of P700 oxidation was not affected by addition of DCMU but was inhibited by HgCl2, an inhibitor of mitochondrial NDH-1, suggesting that P700+ was reduced by electrons from respiratory substrates via plastoquinone (PQ). In the wild-type (WT)
123
72
cells of Synechocystis PCC 6803, transient, complete oxidation of P700 was induced by saturating, white multiple-turnover light but after the reduction of P700+ by electrons from the intersystem chain, P700+ remained at a low level even under background far-red light. In contrast, a high level of P700+ was attained under the same conditions in the NdhB-defective mutant (M55). Thus, the electron donation from the respiratory donor and the photoreductant generated in PSI to P700+ through PQ was observed in the WT cells but not in the M55 mutant (Mi et al. 1992b). These results indicated that NDH-1 is the site of main entry of electrons into the PQ pool in the NDH-1-mediated cyclic electron flow and the respiratory electron flow. Using thylakoid membranes isolated from WT and the M55 mutant of Synechocystis PCC 6803, it was demonstrated that NADPH but not NADH donates electrons to the intersystem chain. In addition, a reconstitution of NADPH- and ferredoxin (Fd)-dependent cyclic electron flow around PS I has been achieved (Mi et al. 1994, 1995). The activity of PS1-cyclic electron transport was strongly impaired in high CO2-grown cells of the DndhD1/D2 double mutant, indicating that ndhD1 and ndhD2 are involved in this activity (Ohkawa et al. 2000). However, low CO2-grown cells of this mutant showed activity similar to the WT cells grown under the same conditions (Zhang et al. 2004). Thus, the presence of ndhD1 and/or ndhD2 is not a prerequisite for the function of PS1-cyclic electron transport. This will be discussed later referring the result of proteomic analysis of NDH-1 complexes from high CO2- and low CO2-grown cells. In contrast to the DndhD3/D4 mutant that was unable to take up CO2, DndhD1/D2 cells took up CO2 and grew normally in air. Thus, ndhD1 and ndhD2 are not involved in CO2 uptake (Ohkawa et al. 2000; Shibata et al. 2001). The NDH-1-dependent PS1-cyclic electron transport is also found in chloroplasts (Shikanai et al. 1998; Burrows et al. 1998). The major PS1-cyclic electron transport in chloroplasts is dependent on pgr5 (Munekage et al. 2002) and contribution of NDH-1dependent cyclic electron transport is relatively small, although it plays an important role especially under stress conditions (Munekage et al. 2004). The homologue of pgr5 is present in Synechocystis PCC 6803 and is involved in antimycinA-sensitive PS1-cyclic electron transport (Yeremenko et al. 2005). The contribution of pgr5-dependent cyclic flow is minor in cyanobacteria.
123
Photosynth Res (2007) 93:69–77
Respiration Respiration and photosynthesis share the same intersystem electron transport carriers in cyanobacteria and NDH-1 is the site of electron donation from the respiratory produced reductants to PQ. Different from bacterial or mitochondrial NDH-1, cyanobacterial NDH-1 uses NADPH but not NADH as substrate (Sandmann and Malkin 1983; Matthijs et al. 1984; Mi et al. 1995; Ma et al. 2006). The reduced PQ is subsequently oxidized by multiple terminal oxidase systems; mainly cyanide-sensitive cytchrome c oxidases (aa3type) and cytochrome bd-type quinol oxidases (Peschek 1980; Howitt and Vermaas 1998) and cyanide insensitive terminal oxidase (ptox) that have been described long ago but have only recently been detected in genomes of a few cyanobacterial strains (Scherer et al. 1988; Rhoads and McIntosh 1991; Josse et al. 2000, 2003). Both M55 and DndhD1/D2 mutants showed low respiration activity and were unable to grow under photoheterotrophic conditions (Ohkawa et al. 2000). In contrast, the DndhD3/D4 mutant showed normal activity of respiration and grew under photoheterotrophic conditions. These results indicated that ndhD1 and/or ndhD2 are essential to respiration and photoheterotrophic growth of cells. There has been reported a contradictory result that an ndhD2-deletion mutant of Synechocystis PCC 6803 showed much higher respiratory activity than the WT (Dzelzkalns et al. 1994). Detailed study on the role of ndhD1 and ndhD2 on respiration is still needed. Chloroplasts also possess the respiratory pathway that couples with photosynthetic electron flow affecting the redox state of PQ, which is called chlororespiration (Bennoun 1982; Casano et al. 2000; Peltier and Cournac 2002). The discovery in higher-plant chloroplasts of a plastid-encoded NAD(P)H-dehydrogenase (Ndh) complex, homologous to the bacterial complex I, and of a nuclear-encoded plastid terminal oxidase (PTOX), homologous to the plant mitochondrial alternative oxidase, brought molecular support to the concept of chlororespiration (Carol et al. 1999; Josse et al. 2000; Joe¨t et al. 2002). In thylakoids of mature chloroplasts, chlororespiration appears to be a relatively minor pathway compared to linear photosynthetic electron flow from H2O to NADP+. However, chlororespiration might play a role in the regulation of photosynthesis by modulating the activity of cyclic electron flow around PS 1.
Photosynth Res (2007) 93:69–77
Other physiological characteristics of mutants defective in NDH-1 The state transitions were strongly inhibited in the M55 mutant (Schreiber et al. 1995). Whether this is a result of low respiratory activity or absence of NDH-1-dependent cyclic electron transport is yet to be clarified. The absence of cyclic electron transport might have caused high sensitivity of the mutant to high NaCl although the mechanism is not clear (Tanaka et al. 1997). In chloroplasts, the PSI-cyclic electron transport mediated by NDH-1 functions in photoprotection. Repeated application of supra-saturating light resulted in severe photo-inhibition and even chlorosis in the ndhB-defective mutant of tobacco, but less effect on the WT (Endo et al. 1999). A remarkable amount of H2O2 was accumulated in leaves of the DndhCKJ mutant of tobacco, which suggested that NDH-1dependent cyclic electron transport functions in alleviating photo-oxidative stress by compensating the stromal over-reduction that induces formation of reactive oxygen species (ROS) (Wang et al. 2006).
Proteomics of cyanobacterial NDH-1 complexes Proteomic analysis of cyanobacterial NDH-1 complexes has revealed the presence of three complexes: NDH-1L (large size), NDH-1M (medium size) and NDH-1S (small size) (Herranen et al. 2004). The NDH-1L complex contains NdhD1 and NdhF1 in addition to NdhA, NdhB, NdhC, NdhE, NdhG, NdhH, NdhI, NdhJ, NdhK, NdhL, NdhM, NdhN and NdhO and is absent in the DndhD1/ndhD2 mutant (Zhang et al. 2004). NDH-1M contains all these subunits except NdhD1 and NdhF1. NDH-1S is composed of four subunits of NdhD3, NdhF3, CupA and CupS. High CO2-grown cells contain predominantly NDH-1L while NDH-1M and NDH-1S are the major complexes in low CO2-adapted cells. A complex (NDH-1MS) containing both NDH-1S and NDH-1M has been isolated from a Thermosynechococcus elongatus strain in which the C terminus of NdhL has been tagged with 6-His. This complex is easily dissociated into NDH-1M and NDH-1S complexes (Zhang et al. 2005). The amount of NDH-1M in the DndhD1/ndhD2 mutant was similar to that of WT either in high CO2 grown (P. Zhang and EM Aro, unpublished) or in low CO2grown cells (Zhang et al. 2004). This indicated that, unlike the NDH-1MS complex, NDH-1L is not
73
converted to NDH-1M but may be decomposed when these membrane subunits are deleted. Electron microscopic observation of NDH-1 complexes isolated from the strain of Thermosynechococcus elongatus with a His-tag on NdhL showed L-shaped NDH-1 complexes with different sizes of hydrophobic region. U-shaped complexes were also observed. The abundance of specific complexes was affected by the CO2 concentration experienced during growth (Arteni et al. 2006). Analysis of various mutants of Synechocystis PCC 6803 for their physiological properties in relation to the presence or absence of NDH-1L, NDH-1M and NDH1S has indicated that NDH-1L is essential to photoheterotrophic growth and the NDH-1MS complex participates in the inducible CO2-uptake system (Zhang et al. 2004). The inhibition of PS1-cyclic electron transport in high CO2-grown cells of the DndhD1/ ndhD2 mutant indicated that NDH-1L is involved in this reaction (Ohkawa et al. 2000). However, low CO2grown cells of this mutant showed the same activity of cyclic electron transport as the WT cells. This led to the conclusion that NDH-1M, the major complex in low CO2 cells of the WT and DndhD1/ndhD2 mutant, is also functioning in cyclic electron transport (Zhang et al. 2004). It is presumed that CupA and CupB may have a CA-like activity and play a role in the conversion of CO2 to HCO-3 but experimental evidence is still missing. CupB has been identified in a band of about 440 kDa after blue native gel electrophoresis but was absent in mutant DndhD4 (M. Xu, T. Ogawa, H. Mi, unpublished). This result suggests that CupB is associated with NdhD4 and NdhF4 to form NDH-1S¢, a homologue of NDH-1S, and is present as a complex of NDH-1MS¢. NDH-1S’ does not contain CupS since its homologues are absent in the strains devoid of the inducible CO2-uptake system.
Active NDH-1 complexes Staining of native gels for NADPH-nitroblue tetrazolium oxidoreductase activity after electrophoresis of ndodecyl-ß-maltoside-treated membranes of Synechocystis sp. strain PCC 6803 revealed several active bands of NDH-1 complexes (Ma et al. 2006). These include a highly active super-complex of NDH-1 (about 1,000 kDa) that was suppressed under low CO2 and a band that was induced under low CO2. These bands appear to be a NDH-1L dimer and NDH-1M, respectively, with subunits essential for the activity.
123
74
Photosynth Res (2007) 93:69–77
Phylogeny of Cyanobacterial NDH-1 complexes and CO2-uptake systems Cyanobacteria have Form 1 (L8S8) Rubisco and are grouped into a-cyanobacteria and b-cyanobacteria based on the Rubisco phylogeny; a-cyanobacteria for those containing Form 1A Rubisco and b-cyanobacteria with Form 1B Rubisco. b-cyanobacteria possess rbcX that encodes putative Rubisco chaperonin, in addition to rbcL and rbcS but rbcX is absent in a-cyanobacteria (Badger et al. 2003; Giordano et al. 2005). Both a- and b-cyanobacteria have carboxysomes that are protein microbodies, consisting of shell proteins and soluble proteins most of which are Rubisco (Beudeker et al. 1980; Price et al. 1992). There are no homologies in many of the shell proteins between a- and b-cyanobacteria. Based on these differences, carboxysomes in b-cyanoabacteria associated with Form 1B Rubisco are termed b-carboxysomes and those in a-cyanobacteria associated with Form 1A
Rubisco as a-carboxysomes. It is considered that the acyanobacterial lineage was branched from the b-cyanobacterial lineage at an early stage of evolution. All the genes that encode 15 subunits of NDH-1L complex (ndhA, ndhB, ndhC, ndhD1, ndhE, ndhF1, ndhG, ndhH, ndhI, ndhJ, ndhK, ndhL, ndhM, ndhN and ndhO) are found in the genomes of the 17 cyanobacterial strains except that ndhL and ndhD2 are absent in Gloeobacter (Fig. 1). This suggests that all the ndh genes were present in an ancestor of cyanobacteria at an early stage of evolution and Gloeobacter might have lost ndhL and ndhD2 after branching. The presence of genes involved in inducible and constitutive CO2-uptake systems in Gloeobacter suggests that both CO2-uptake systems were present in an ancestor before the branching of Gloeobacter. However, the absence of ndhL suggests that the activity of CO2-uptake systems is very weak in Gloeobacter, as the inactivation of ndhL in Synechocystis PCC 6803 strongly reduced the CO2-uptake activity (Ogawa 1991b, 1992).
NDH-1L/NDH-1M Strains
CO2 uptake systems
NdhA,B,C,E,G, NdhD1F1 NdhD2 NdhL NdhD3F3 NdhD4F4 H,I,J,K,M,N,O
CupAS
CupB
Gloeo
β-cyanobacteria
Thermo Syn6803 Cw8501 Tric101 Np29133 Ana7120 Av29413 Syn6301 Syn7942
α-cyanobacteria
Syn9902 Syn8102 Syn9605 Pro9313 Pro120 ProMED4 Pro9312
Fig. 1 The presence (shadowed) or absence (blank) of genes encoding subunits of NDH-1 complexes, in 17 cyanobacterial strains. Marine strains are shadowed. Genome sequences were obtained from the sites of http://www.kazusa.or.jp/cyano/ and http://genome.jgi-psf.org/mic_home.html. Abbreviations for the strains are: Gloeo (Gloeobacter violaceus PCC 7421), Thermo (Thermosynechococcus elongatus BP-1), Syn6803 (Synechocystis sp. PCC 6803), Cw8501 (Crocosphaera watsonii WH 8501), Tric101 (Trichodesmium erythraeum IMS101), Np29133 (Nostoc
123
punctiforme ATCC 29133), Ana7120 (Anabaena sp. PCC 7120), Av29413 (Anabaena variabilis ATCC 29413), Syn6301 (Synechococcus sp. PCC 6301), Syn7942 (Synechococcus elongatus PCC 7942), Syn8102 (Synechococcus sp. WH8102), Syn9605 (Synechococcus sp. CC9605), Syn9902 (Synechococcus sp. CC9902), Pro9313 (Prochlorococcus marinus MIT 9313), Pro120 (Prochlorococcus marinus SS120), ProMED4 (Prochlorococcus marinus MED4), Pro9312 (Prochlorococcus marinus sp. MIT 9312)
Photosynth Res (2007) 93:69–77
All the a-cyanobacterial strains do not have an inducible CO2-uptake system, which might have been lost after the early branching of the a-cyanobacterial lineage. The absence of both CO2-uptake systems in Prochlorococcus strains indicates that the genes involved in the constitutive CO2-uptake system were lost after the branching of the Prochlorococcus lineage. Most of the b-cyanobacterial species possess both inducible and constitutive CO2-uptake systems. However, two marine species, Crocosphaera watsonii strain WH8501 and Trichodesmium erythraeum IMS101, do not have inducible CO2-uptake system. Acknowledgements This work was partially supported by grants to HM from the National Natural Science Foundation of China (No. 30470151 and No. 90306013) and in part supported by a grant to TO by the Membrane Biology EMSL Scientific Grand Challenge Project at the W. R. Wiley Environmental Molecular Sciences Laboratory, a national scientific user facility sponsored by the US Department of Energy Office of Biological and Environmental Research program located at Pacific Northwest National Laboratory. Pacific Northwest National Laboratory is operated for the Department of Energy by Battelle.
References Arteni AA, Zhang P, Battchikova N et al (2006) Structural characterization of NDH-1 complexes of Thermosynechococcus elongatus by single particle electron microscopy. Biochim Biophys Acta 1757:1469–1475 Badger MR, Price GD, Long BM et al (2003) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57:249–265 Battchikova N, Zhang P, Rudd S et al (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1M complexes of Synechocystis sp PCC 6803. J Biol Chem 280:2587–2595 Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79:4352–4356 Beudeker R, Cannon GC, Kuenen JG et al (1980) Relations between RuBP carboxylase, carboxysomes and CO2 fixing capacity in the obligate chemolithotroph Thiobacillus neapolitana grown under different limitations in the chemostat. Arch Microbiol 1241:185–189 Burrows PA, Sazanov LA, Svab Z et al (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876 Carol P, Stevenson D, Bisanz C et al (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57–68 Casano LM, Zapata JM, Martin M et al (2000) Chlororespiration and poising of cyclic electron transport—Plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. J Biol Chem 275:942–948 Deng Y., Ye J, Mi H (2003a) Effects of low CO2 on NAD(P)H dehydrogenase, a mediator of cyclic electron transport around photosystem I in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 44:534–540
75 Deng Y, Ye J, Mi H et al (2003b) Response of NAD(P)H dehydrogenase complex to the alteration of CO2 concentration in the cyanobacterium Synechocystis PCC 6803. J Plant Physiol 160:967–970 Dzelzkalns VA, Obinger C, Regelsberger G et al (1994) Deletion of the structural gene for the NADH-dehydrogenase subunit of Synechocystis 6803 alters respiratory properties. Plant Physiol 106:1435–1442 Endo T, Shikanai T, Takabayashi A et al (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett 457:5–8 Figge RM, Cassier-Chauvat C, Chauvat F et al (2001) Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress. Mol Microbiol 39:455–468 Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1–5 Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131 Herranen M, Battchikova N, Zhang P et al (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp PCC 6803. Plant Physiol 134:470–481 Hihara Y, Kamei A, Kanehisa M et al (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793–806 Howitt CA, Vermaas WFJ (1998) Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 37:17944–17951 Joe¨t T, Cournac L, Peltier G et al (2002) Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADHdehydrogenase complex. Plant Physiol 128:760–769 Josse EM, Alcaraz JP, Laboure´ AM et al (2003) In vitro characterization of a plastid terminal oxidase (PTOX). Eur J Biochem 270:3787–3794 Josse EM, Simkin AJ, Gaffe J et al (2000) A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol 123:1427–1436 Kaneko T, Sato S, Kotani H et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136 Kaplan A, Reinhold L (1999) The CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50:539–570 Klughammer B, Sultemeyer D, Badger MR et al (1999) The involvement of NAD(P)H dehydrogenase subunits, NdhD3 and NdhF3, in high-affinity CO2 uptake in Synechocystis sp. PCC 7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria. Mol Microbiol 32:1305– 1315 Ma W, Deng Y, Ogawa T et al (2006) Active NDH-1 complexes from the cyanobacterium Synechocystis sp Strain PCC 6803. Plant Cell Physiol 47:1432–1436 Ma W, Mi H (2005) Expression and activity of type-1 NAD(P)H dehydrogenase at different growth phases of cyanobacterium, Synechocystis PCC 6803. Physiol Plant 125:135–140 Maeda S, Badger MR, Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the
123
76 cyanobacterium, Synechococcus sp. PCC 7492. Mol Microbiol 43:425–435 Matthijs HCP, Lude´rus EME, Lo¨ffler HJM et al (1984) Energy metabolism in the cyanobacterium Plectonema boryanum. Participation of the thylakoid photosynthetic electron transfer chain in the dark respiration of NADPH and NADH. Biochim Biophys Acta 766:29–37 Mi H, Endo T, Schreiber U et al. (1992a) Donation of electrons from cytosolic components to the intersystem chain in the cyanobacterium Synechococcus sp. PCC 7002 as determined by reduction of P700+. Plant Cell Physiol 33:1099–1105 Mi H, Endo T, Schreiber U et al (1992b) Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33:1233–1237 Mi H, Endo T, Schreiber U et al (1994) NAD(P)H-dehydrogenase-dependent cyclic electron flow around photosystem I in the cyanobacterium Synechocystis PCC 6803: a study of dark-starved cells and spheroplasts. Plant Cell Physiol 35:163–173 Mi H, Endo T, Ogawa T et al (1995) Thylakoid membranebound pyridine nucleotide dehydrogenase complex mediated cyclic electron transport in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 36:661–668 Mi H, Deng Y, Tanaka Y et al (2001) Photo-induction of an NADPH dehydrogenase which functions as a mediator of electron transport to the intersystem chain in the cyanobacterium Synechocystis PCC 6803. Photosynth Res 70:167–173 Munekage Y, Hashimoto M, Miyake C et al (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582 Munekage Y, Hojo M, Meurer J et al (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371 Munshi MK, Kobayashi Y, Shikanai T (2005) Identification of a novel protein, CRR7, required for the stabilization of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant J 44:1036–1044 Munshi MK, Kobayashi Y, Shikanai T (2006) Chlororespiratory reduction 6 is a novel factor required for accumulation of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Physiol 141:737–744 Ogawa T (1990) Mutants of Synechocystis PCC 6803 defective in inorganic carbon transport. Plant Physiol 94:760–765 Ogawa T (1991a) A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC 6803. Proc Natl Acad Sci USA 88:4275–4279 Ogawa T (1991b) Cloning and inactivation of a gene essential to inorganic carbon transport of Synechocystis PCC 6803. Plant Physiol 96:280–284 Ogawa T. (1992). Identification and characterization of the ictA/ ndhL gene product essential to inorganic carbon transport of Synechocystis PCC 6803. Plant Physiol 99:1604–1608 Ohkawa H, Pakrasi HB, Ogawa T (2000) Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp strain PCC 6803. J Biol Chem 275:31630–31634 Ohkawa H, Sonoda M, Katoh H et al (1998) The use of mutants in the analysis of the CCM in cyanobacteria. Can J Bot 76:1035–1042 Ohkawa H, Sonoda M, Shibata M et al (2001) Localization of NAD(P)H dehydrogenase in the cyanobacterium Synechocystis sp strain PCC 6803. J Bacteriol 183:4938–4939 Omata T, Price GD, Badger MR et al (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate
123
Photosynth Res (2007) 93:69–77 uptake in the cyanobacterium Synechococcus sp strain PCC7492. Proc Natl Acad Sci USA 96:13571–13576 Peltier G, Cournac L (2002) The chlororespiration. Ann Rev Plant Biol 53: 523–550 Peschek GA (1980) Electron transport reactions in respiratory particles of hydrogenase-induced Anacystis nidulans. Arch Microbiol 125:123–131 Price GD, Coleman JR, Badger MR (1992) Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC 7942. Plant Physiol 100:784–793 Price GD, Woodger FJ, Badger MR et al (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101:18228–18233 Prommeenate P, Lennon AM, Markert C et al (2004) Subunit composition of NDH-1 complexes of Synechocystis sp. PCC 6803: identification of two new ndh gene products with nuclear-encoded homologues in the chloroplast Ndh complex. J Biol Chem 29:28165–2873 Rhoads DM, McIntosh L (1991) Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott). Proc Natl Acad Sci USA 88:2122–2126 Rumeau D, Becuwe-Linka N, Beyly A et al (2005) New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17:219–232 Sandmann G, Malkin R (1983) NADH and NADPH as electron donors to respiratory and photosynthetic electron transport in the blue-green alga, Aphanocapsa. Biochim Biophys Acta 725:221–224 Scherer S, Ha¨fele U, Kru¨ger GHJ et al (1988) Respiration, cyanide-insensitive oxygen uptake and oxidative photophosphorylation in cynobacteria. Physiol Plant 72:379–384 Schreiber U, Endo T, Mi H et al (1995) Quenching analysis of chlorophyll fluorescence by the saturation pulse method: Particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol 36:873–882 Shibata M, Katoh H, Sonoda M et al (2002a) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277:18658– 18664 Shibata M, Ohkawa H, Kaneko T et al (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98:11789–11794 Shibata M, Ohkawa H, Katoh H et al (2002b) Two CO2 uptake systems in cyanobacteria: four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC 6803. Funct Plant Biol 29:123–129 Shikanai T, Endo T, Hashimoto T et al (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95:9705–9709 Tanaka Y, Katada S, Ishikawa H et al (1997) Electron flow from NAD(P)H dehydrogenase to photosystem I is required for adaptation to salt shock in the cyanobacterium Synechocystis sp PCC 6803. Plant Cell Physiol 38:1311–1318 Tchernov D, Helman Y, Keren N et al (2001). Passive entry of CO2 and its energy-dependent intracellular conversion HCO-3 in cyanobacteria are driven by a photosystem I-generated DlH+. J Biol Chem 276:23450–23455 Volokita M, Zenvirth D, Kaplan A et al (1984) Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis. Plant Physiol 76:599–602
Photosynth Res (2007) 93:69–77 Wang P, Duan W, Takabayashi A et al (2006) Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiol 41:465–474 Wang HL, Postier BL, Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279:5739– 5751 Yeremenko N, Jeanjean R, Prommeenate P et al (2005) Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobac-
77 terium Synechocystis sp PCC 6803. Plant Cell Physiol 46:1433–1436 Zhang P, Battchikova N, Jansen T et al (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/ Sll1735 in Synechocystis sp PCC 6803. Plant Cell 16:3326– 3340 Zhang P, Battchikova N, Paakkarinen V et al (2005) Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem J 390:513–520
123
