In: Photosynthesis ISBN 978-1-60692-719-9 Editors: Th. B. Buchner and N. H. Ewingen, pp. © 2009 Nova Science Publishers, Inc.

Chapter 9

MULTIPLICITY OF NDH-1 COMPLEXES IN CYANOBACTERIA

Weimin Ma1,*, Hualing Mi2

1College of Life and Environment Sciences, Shanghai Normal University, Guilin Road 100, Shanghai, 200234, China

2National Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences,

Fenglin Road 300, Shanghai, 200032, China

ABSTRACT

Cyanobacterial NADPH dehydrogenase (NDH-1) was identified more than 16 years ago. This enzyme is confined to the thylakoid membrane, and it accepts electrons from NADPH and contains at least 15 subunits. Recently, studies using reverse genetics, proteomics, and activity staining have shown the presence of functionally distinct multiple NDH-1 complexes in cyanobacterial cells. In this mini-review, these cyanobacterial NDH-1 complexes will be described with emphasis placed on their multiplicity and assembly. (1) Firstly, reverse genetic studies proposed the presence of 2 functionally distinct NDH-1 complexes in cyanobacteria; (2) subsequently, proteomic studies revealed the presence of multiple functionally distinct NDH-1 complexes in the cyanobacterial thylakoid membrane, including NDH-1L (large size; 460 kDa), NDH-1M (middle size; 330 kDa) and NDH-1S (small size; 190 kDa). However, none of these NDH-1 complexes showed NADPH dehydrogenase activity. (3) Recently, activity staining studies identified 2 active NDH-1 complexes in a unicellular cyanobacterium. Based on the size, the 2 active NDH-1 complexes were called Act-NDH-1Sup (active supercomplex; approximately 1,000 kDa) and Act-NDH-1M (active mediumcomplex; approximately 380 kDa). Act-NDH-1Sup is a newly identified complex, and its protein activity is much higher than that of Act-NDH-1M. It is also more than twice the size of NDH-1L, while Act-NDH-1M is similar in size to NDH-1M. In addition, both Act-NDH-

* Author for correspondence. Tel: +86 21 64321617; Fax: +86 21 64322931; E-mail: cyanoma@hotmail.com

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1Sup and NDH-1L participate in cellular respiration, while both Act-NDH-1M and NDH-1M are involved in CO2 uptake. Thus, from the analysis of the sizes and physiological functions of these 4 cyanobacterial NDH-1 complexes, it is speculated that Act-NDH-1Sup is an NDH-1L dimer with still unknown activity subunit(s), and that Act-NDH-1M is an active NDH-1M analog. However, the active component(s) and the electron input device of these cyanobacterial NDH-1 complexes has remained undocumented.

Keywords: Cellular respiration; CO2 uptake; cyanobacteria; cyclic electron transport around photosystem I; multiple NADPH dehydrogenase complexes

ABBREVIATIONS D1/D2, ΔndhD1/D2; M55, ΔndhB; NDH-1, NADPH dehydrogenase; PSI, photosystem I; PSII, photosystem II; Synechocystis 6803, Synechocystis sp. strain PCC 6803; T. elongatus, Thermosynechococcus elongatus BP-1; WT, wild-type

OVERVIEW The proton-translocating NAD(P)H:quinone oxidoreductase (NDH-1; also called

complex I) is found in most species spanning from bacteria to mammals (Friedrich et al., 1995; Yagi et al., 1998; Friedrich et al., 2000; Brandt et al., 2003). The general function of this enzyme is to transfer electrons from an electron donor (usually NADH) to quinone in order to generate a proton motive force used for ATP synthesis.

Complex I (NDH-1) is a multisubunit enzyme, and it contains a flavin mononucleotide (FMN) and several iron-sulfur (Fe-S) clusters (Friedrich et al., 1995). The respiratory complex I (NDH-1) from Escherichia coli is composed of 14 subunits (Friedrich, 1998), 11 of which were identified in cyanobacteria and chloroplasts (i.e., NdhA-K; Figure 1); however, 3 subunits (NuoE, F and G) involved in accepting electrons from NADH in E. coli are missing from cyanobacterial and chloroplastic NDH-1 (Friedrich and Scheide, 2000; Figure 1). The NuoF subunit contains FMN and may have an NADH-binding site (Figure 1), thus, the three subunits have been referred to as the NADH-binding domain (Friedrich, 1998). The absence of homologous genes from the NuoE, NuoF and NuoG subunits in cyanobacteria and chloroplasts implies that cyanobacterial and chloroplastic NDH-1 has a unique NAD(P)H-binding domain for photosynthetic organisms.

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Figure 1. A scheme for the structure of cyanobacterial/chloroplastic NDH-1 compared with complex I in E. coli. The complex I/NDH-1 complex was composed of an activity domain, a connecting domain and a membrane domain. Subunits labeled by black letters are homologous between complex I and NDH-1, and those with white letters (NdhL, M, N, and O) are specific to NDH-1 in photosynthetic organisms. The arrangement of the subunits of complex I corresponds to the homologous NDH-1 ones. The activity domain (NuoE, F and G) in E. coli is missing in cyanobacterial and chloroplastic NDH-1, and is indicated by three question marks. CM, cytoplasmic membrane; TM, thylakoid membrane.

Recently, proteomic studies of NDH-1 complexes have identified 4 new subunits (NdhL, M, N, and O) in cyanobacterial NDH-1 (Prommeenate et al., 2004; Zhang et al., 2004; Battchikova et al., 2005) which are also found in chloroplastic NDH-1 (Rumeau et al., 2005; Shimizu et al., 2008). In addition, several genes have been indicated in the encoding of new subunits of Arabidopsis NDH-1 (Munshi et al., 2005), and their homologues are also found in cyanobacterial genomes (Ogawa and Mi, 2007). The aforementioned newly identified NDH-1 subunits are all unique to cyanobacteria and plants, and are not found in heterotrophic organisms (Endo et al., 2008; see Figure 1). Taken together, this implies that the NDH-1 in cyanobacteria and chloroplasts should be referred to as “photosynthetic NDH-1,” which has a unique structure and function distinguishable from “respiratory NDH-1.”

Cyanobacterial NDH-1 was first discovered more 16 years ago in the Synechocystis sp. strain PCC 6803 (hereafter Synechocystis 6803; Berger et al., 1991, 1993). This enzyme is confined to the thylakoid membrane (Ohkawa et al., 2001) and accepts electrons from NADPH (Mi et al., 1995; Ma et al., 2006). The NDH-1 in cyanobacteria is essential for cellular respiration and cyclic electron transport around photosystem I (cyclic PSI), which are 2 common physiological functions with chloroplastic NDH-1 (Ogawa 1991a; Mi et al., 1992b; Burrows et al., 1998; Casano et al., 2000; Shikanai and Endo, 2000; Joët et al., 2002; Peltier and Cournac, 2002; Munekage et al., 2004; Braun and Zabaleta, 2007). Interestingly, cyanobacterial NDH-1 also participates in CO2 uptake, which is specific to cyanobacteria but not to chloroplasts (Ogawa 1991a, b, 1992).

Recent studies using reverse genetics, proteomics and activity staining have revealed the presence of functionally distinct multiple NDH-1 complexes in cyanobacterial cells (Matsuo et al., 1998; Ohkawa et al., 2000; Shibata et al., 2001; Maeda et al., 2002; Deng et al., 2003a, b; Herranen et al., 2004; Prommeenate et al., 2004; Zhang et al., 2004, 2005; Ma et al., 2006). In this mini-review, these cyanobacterial NDH-1 complexes will be described with emphasis on their multiplicity and assembly. For more comprehensive knowledge regarding cyanobacterial NDH-1 complexes, the reader may refer to earlier reviews (for review, see

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Friedrich et al., 1995; Friedrich and Scheide, 2000; Ogawa and Kaplan, 2003; Battchikova and Aro, 2007; Ogawa and Mi, 2007).

TWO TYPES OF NDH-1 AS REVEALED BY REVERSE GENETICS

From the analysis of the entire genomic sequence of Synechocystis 6803, it was found

that at least 4 ndhD genes (ndhD1-D4) and 3 ndhF genes (ndhF1, F3 and F4) are present in this cyanobacterium, although most of the other ndh genes are present as a single copy (Kaneko et al., 1996; http://www.kazusa.or.jp/cyano/). Reverse genetic studies using various ΔndhD mutants showed that one double mutant, ΔndhD1/ndhD2, was unable to survive under photoheterotrophic conditions, although it could take up CO2 in the light and grow normally under air levels of CO2; the other double mutant, ΔndhD3/ndhD4, could grow under photoheterotrophic conditions but was unable to take up CO2 and to grow in air at pH 7.0 (Ohkawa et al., 2000). The opposite phenotypes of the 2 ΔndhD double mutants not only revealed the effect of various NdhD subunits on the physiological function of cyanobacterial NDH-1 complexes, but also first indicated the presence of two functionally distinct types of NDH-1 in Synechocystis 6803, i.e., one containing NdhD1 and/or NdhD2 which participates in cell respiration and the other including NdhD3 and/or NdhD4 which is involved in CO2 uptake.

A phylogenic analysis has indicated that the cyanobacterial ndhD1/ndhD2 and ndhF1 genes are highly homologous to the chloroplastic ndhD and ndhF genes, respectively (Shibata et al., 2001). However, the ndhD3/ndhD4 and ndhF3/ndhF4 genes are absent in chloroplastic genomes which suggests that CO2 uptake systems dependent on these genes are present only in cyanobacteria.

MULTIPLE NDH-1 COMPLEXES AS REVEALED BY PROTEOMICS Although reverse genetic studies have demonstrated that at least 2 functionally distinct

NDH-1 complexes are present in the thylakoid membrane of Synechocystis 6803 (Ohkawa et al., 1998, 2000; Price et al., 1998; Klughammer et al., 1999; Shibata et al., 2001; Maeda et al., 2002), little is known regarding their properties.

Recently, proteomic studies first revealed the presence of several functionally distinct NDH-1 complexes, NDH-1L (large size; 460 kDa), NDH-1M (middle size; 330 kDa), and NDH-1S (small size; 190 kDa), in the thylakoid membrane of Synechocystis 6803 (Herranen et al., 2004). In addition, NDH-1MS (490 kDa), NDH-1L, and NDH-1S were identified in Thermosynechococcus elongatus BP-1 (T. elongatus; Zhang et al., 2005). Further, single particle electron microscopic analysis of thylakoid proteins from T. elongatus enabled visualization of the L-shaped NDH-1L and NDH-1M, and the U-shaped NDH-1MS (Arteni et al., 2006; Folea et al., 2008). The NDH-1L complex contains NdhD1 and NdhF1 in addition to NdhA, NdhB, NdhC, NdhE, NdhG, NdhH, NdhI, NdhJ, and NdhK as well as the newly identified subunits (NdhL, NdhM, NdhN, and NdhO) (Zhang et al., 2004; Battchikova et al., 2005) and appears to be identical to NDH-1A as reported by Prommeenate et al. (2004). All these subunits, except NdhD1 and NdhF1, are present in NDH-1M. NDH-1S includes

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NdhD3, NdhF3, CupA, and CupS (Herranen et al., 2004; Ogawa and Mi, 2007). On the other hand, CupB has been identified in a NDH-1 complex of approximately 450 kDa but is absent in ΔndhD4 and ΔndhF4 mutants (Xu et al., 2008). This implies 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’ (Battchikova and Aro, 2007; Ogawa and Mi, 2007). However, a complex such as NDH-1MS’ has not been detected by either 2D-gel electrophoresis or single particle electron microscopic analysis. Also, none of these purified and/or otherwise identified cyanobacterial NDH-1 complexes mentioned above showed NADH/NADPH dehydrogenase activity.

Cyanobacterial NDH-1 complexes are involved in CO2 uptake (Ogawa, 1991a, b, 1992), cyclic PSI and cellular respiration (Mi et al., 1992a, b, 1994, 1995). Although the mechanism of CO2 uptake is not yet known, it is postulated that CO2 enters the cells by diffusion and is converted to HCO3

– by the NDH-1 complex (Kaplan and Reinhold, 1999; Tchernov et al., 2001) localized on the thylakoid membrane (Ohkawa et al., 2001; Zhang et al., 2004). Analysis of various mutants of Synechocystis 6803 for their physiological properties in relation to the presence or absence of NDH-1L, NDH-1M, and NDH-1S indicated that NDH-1L is essential for cellular respiration and photoheterotrophic growth, whereas NDH-1MS participates in high affinity CO2 uptake in Synechocystis 6803 (Zhang et al., 2004).

TWO ACTIVE NDH-1 COMPLEXES AS REVEALED BY ACTIVITY STAINING

The purification and identification of active cyanobacterial NDH-1 complexes is an

important step toward studying their functional properties and better understanding the bioenergetics of the thylakoid membrane. Thus, many works have been made in order to purify and identify the active cyanobacterial NDH-1 complexes since 1993, and the main progress is summarized as follows: (1) Berger et al. (1993) first described an isolation of the NDH-1 subcomplex consisting of several peripheral subunits, but the complex was functionally inactive; (2) Matsuo et al. (1998) purified an active NDH-1 subcomplex of 376 kDa but 2 membrane subunits (NdhA and NdhB) were not detected in this complex; (3) Deng et al. (2003a) isolated 2 active NDH-1 subcomplexes of about 200-250 kDa including the hydrophobic NdhA subunit.

Recently, the activity of NDH-1 was found to be strongly affected by the growth phase of cells, and was highest in cells in the logarithmic phase of growth (Ma and Mi, 2005). Thus, cyanobacterial cells in the logarithmic phase were utilized and success was achieved in identifying active NDH-1 complexes. Analysis of staining of native gels for NADPH-nitroblue tetrazolium (NBT) oxidoreductase activity after electrophoresis of n-dodecyl-β-maltoside (DM)-treated membranes of wild-type (WT) Synechocystis 6803 and its specific ndh gene knockout mutants ΔndhB (M55) and ΔndhD1/D2 (D1/D2) and immunoblotting of these active bands using various antibodies of NDH-1 membrane and peripheral subunits demonstrated the presence of 2 major active NDH-1 complexes in the unicellular cyanobacterium (Ma et al., 2006). Based on the size, the 2 active NDH-1 complexes were called Act-NDH-1Sup (active supercomplex; approximately 1,000 kDa) and Act-NDH-1M (active mediumcomplex; approximately 380 kDa). Act-NDH-1Sup is a newly identified

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complex and its protein activity is much higher than that of Act-NDH-1M (Ma et al., 2006). In contrast, Act-NDH-1M is similar to complexes previously identified by Matsuo et al. (1998) and Deng et al. (2003b).

Interestingly, further research showed that the different properties of the 2 active NDH-1 complexes were responsive to the signals of environment and the levels of nutrition, and the main points are summarized as follows: (1) Ma et al. (2006) demonstrated that low CO2 markedly suppressed the activity of Act-NDH-1Sup, while it significantly stimulated that of Act-NDH-1M; (2) both the redox changes of the plastoquinone (PQ) pool and the levels of exogenous glucose regulated the expression and activity of Act-NDH-1Sup, but not of Act-NDH-1M (Ma et al., 2008a, b).

From the analysis of the relationship between the activities of Act-NDH-1Sup and Act-NDH-1M and the rates of electron transport mediated by these 2 complexes in WT Synechocystis 6803 cells grown at high and low CO2, respectively (Table 1), it was found that Act-NDH-1Sup participates in cellular respiration, while Act-NDH-1M is involved in cyclic PSI; this was confirmed through analysis of the other correlation between the activities of Act-NDH-1Sup and Act-NDH-1M as well as the rates of electron transport mediated by these 2 complexes in high CO2-grown M55 and low CO2-grown D1/D2 mutants, respectively (Table 1). In addition, Ma et al. (2006) have reported a significant stimulation of the staining activity of Act-NDH-1M, but not Act-NDH-1Sup under low CO2 conditions, and indicating that Act-NDH-1M, but not Act-NDH-1Sup, participates in CO2 uptake.

Recently, the roles of Act-NDH-1Sup and Act-NDH-1M were investigated under heat stress. The results indicated that Act-NDH-1Sup is essential in alleviating the heat-induced inhibition of PSII-driven electron transport rate (ETR), while Act-NDH-1M is required to accelerate the heat-induced stimulation of PSI-driven ETR. The former is most likely caused by diverting excess electrons and consequently, reducing the generation of reactive oxygen species (ROS) via this active NDH-1 supercomplex-mediated respiratory electron transport pathway; the latter is most likely caused by synthesizing the extra ATP via this active NDH-1 mediumcomplex-mediated cyclic PSI (Ma et al., 2008c).

Table 1. The relationship between the activities of Act-NDH-1Sup and Act-NDH-1M

and the rates of electron transport mediated by these 2 complexes in wild-type Synechocystis 6803 (WT), and its ΔndhB (M55), ΔndhD1/D2 (D1/D2) mutants grown at

high and low CO2, respectively

Active NDH-1 complexes Rates of electron transport Strain CO2 levels

Act-NDH-1Sup Act-NDH-1M Respiration Cyclic PSI High CO2 ++ +/- ++ +/-

WT Low CO2 +/- ++ +/- ++

M55 High CO2 - - +/- +/- D1/D2 Low CO2 - ++ +/- ++

++, strong; +, moderate; +/-, poor; -, none (not detected).

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A HYPOTHETICAL SCHEME OF THE ASSEMBLY OF MULTIPLE NDH-1 COMPLEXES IN CYANOBACTERIA

The absence of Act-NDH-1Sup in the D1/D2 mutant indicates that this complex contains

NdhD1 and/or NdhD2, and is similar in composition to NDH-1L (Herranen et al., 2004; Zhang et al., 2004; Ma et al., 2006). However, it is more than twice the size of NDH-1L and is closer in size to the NDH-1 supercomplex found in maize chloroplasts (Darie et al., 2005). Further, the NDH-1 supercomplex which is highly active in NADPH oxidation has been identified in spinach and tobacco chloroplasts (Mi, H., unpublished data), which indicates that the presence of Act-NDH-1Sup appears to be common in cyanobacteria and chloroplasts. However, Act-NDH-1M is similar in size to NDH-1M. The Act-NDH-1Sup complex and NDH-1L participate in cellular respiration, while Act-NDH-1M and NDH-1M are involved in CO2 uptake. Taken together, it appears that Act-NDH-1Sup and Act-NDH-1M are an NDH-1L dimer and an NDH-1M analog, respectively, with subunit(s) essential for activity. A hypothetical scheme of the assembly of multiple NDH-1 complexes in cyanobacteria is shown in Figure 2.

As shown in Figure 2, the differences in the multiple NDH-1 complexes primarily depend on the presence or absence of activity subunit(s) and/or NdhD1 and NdhF1. The dissociation of the dimeric structure and activity subunit(s) or NdhD1 and NdhF1 from the highly active Act-NDH-1Sup generates the inactive NDH-1L or the active Act-NDH-1M; the cleavage of activity subunit(s) from Act-NDH-1M complex produces an inactive NDH-1M (Figure 2). Act-NDH-1M does not contain NdhD1 or NdhD2 but it does show NADPH oxidation activity (Ma et al., 2006). NdhF might be also absent in Act-NDH-1M, since this subunit is present next to NdhD on the outer side of the complex (Casano et al., 2004). In addition, NDH-1L, which includes NdhD1 and NdhF1, does not show NADPH oxidation (Herranen et al., 2004; Zhang et al., 2004, 2005). This indicates that neither NdhD nor NdhF are essential for NADPH oxidation. Although a dimeric structure may be important in achieving the high activity of Act-NDH-1Sup, it is not a prerequisite for the activity as seen in the case of Act-NDH-1M (monomeric) described in Figure 2.

PERSPECTIVE Although much progress has been made toward revealing the multiplicity of the

cyanobacterial NDH-1 complexes, including the characterization of their structural compositions and physiological functions, the question of whether or not the presence of other yet unidentified NDH-1 complexes in cyanobacterial cells and their assembly is worthy of further investigation (Figure 2). In addition, to better characterize these cyanobacterial NDH-1 complexes, there are many questions need to be answered in the future, and the major points are summarized as follows.

The absence of homologous genes from the active NuoE, NuoF, and NuoG subunits of E. coli in cyanobacterial and chloroplastic NDH-1 complexes (see Figure 1) has given rise to the most important question: Why do catalytically active subunits of cyanobacterial and chloroplastic NDH-1 complexes differ so remarkably from these corresponding proteins performing the similar diaphorase function in NDH-1 complexes of non-photosynthetic

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organisms? The identification of these subunits in cyanobacteria would be a significant step forward in understanding the bioenergetics of the thylakoid membrane. Conversely, if such subunits do not exist in cyanobacterial NDH-1 complexes, what is the reaction mechanism and how are electrons donated to the NDH-1 complex? Recent studies using the yeast two-hybrid method showed the presence of weak but positive protein-protein interactions in the ferredoxin-NADP+ oxidoreductase (FNR) and the 3 newly identified subunits, NdhM, NdhN and NdhO, in Synechocystis 6803 cells (Zhang, J. and Ma, W., unpublished data), implying that the FNR may supply electrons from NADPH to the cyanobacterial NDH-1 complex; this was proposed in chloroplasts as well (Guedeney et al., 1996; Quiles and Cuello, 1998; Quiles et al., 2000). To confirm this theory, further investigation regarding the interaction between the FNR and the NDH-1 complex should be carried out. However, if the presence of such weak protein-protein interactions between the FNR and NDH-1 complex is confirmed, what is the protein factor that binds the FNR with the complex? Further proteomic studies might reveal the full structure of this complex, including the protein factor that binds the FNR and activity subunits.

Figure 2. A hypothetical scheme of the assembly of multiple NDH-1 complexes in cyanobacteria. The assembly of the four NDH-1 complexes was based on the results of reverse genetics experiments. Act-NDH-1Sup and NDH-1L participate in cellular respiration, while Act-NDH-1M and NDH-1M are involved in CO2 uptake. Of these four complexes, Act-NDH-1Sup and Act-NDH-1M were attributed to the activity of NDH-1 and the former is a highly active NDH-1 supercomplex; however, neither NDH-1L nor NDH-1M showed NADPH oxidation activity. The size of Act-NDH-1Sup was more than twice that of NDH-1L, and Act-NDH-1M was similar in size to NDH-1M, suggesting that Act-NDH-1Sup and Act-NDH-1M are an NDH-1L dimer and an NDH-1M analog, respectively, with subunit(s) essential for activity. The hypothetical domain responsible for the dehydrogenase activity is indicated by three question marks. TM, thylakoid membrane.

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Recently, the hydrophilic domain of respiratory complex I from Thermus thermophilus has been purified and its crystal structure has been solved at 3.3 Å resolution (Sazanov and Hinchliffe, 2006). However, the purification of intact and homogeneous cyanobacterial NDH-1 complexes remains elusive; thus, it appears that one of the most important future tasks is to develop a technique to purify these active NDH-1 complexes in order to study their enzymatic properties, subunit compositions, and 3-D structures as well as to validate the results of reverse genetic studies at the protein level.

ACKNOWLEDGEMENTS We thank Dr. T Ogawa, retired professor of Nagoya University and visiting professor of

the Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, for fruitful discussion. This work was partially supported by the National Natural Science Foundation of China (No. 30770175), the Shanghai Natural Science Foundation (No. 07ZR14086), the Innovation Program of Shanghai Municipal Education Commission (No. 08ZZ67), the Leading Academic Discipline Project of Shanghai Municipal Education Commission (No. J50401), and the Key Fundamental Project of Shanghai (No. 06JC14091).

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