"Membrane-Bound Protein Complexes for Photosynthesis and ...

Membrane-Bound Protein Complexes for Photosynthesis and Respiration in Cyanobacteria Aparna Nagarajan,

Advanced article Article Contents • Introduction • Energy Transfer by Antenna Complexes • Reaction Centres and Photosynthetic Electron Transport • Respiratory Electron Transport • Components Shared between Photosynthesis and Respiration • Regulation of Photosynthesis and Respiration • Acknowledgements

Department of Biology, Washington University, St. Louis, Online posting date: 15th June 2016

Missouri, USA

Himadri B Pakrasi,

Department of Biology, Washington University, St. Louis,

Missouri, USA Based in part on the previous version of this eLS article ‘Photosynthesis and Respiration in Cyanobacteria’ (2001) by Wim FJ Vermaas.

Cyanobacteria are the evolutionarily oldest organisms with the capability of evolving oxygen, giving rise to the present day atmosphere. These prokaryotic microorganisms have the unique ability to perform oxygenic photosynthesis and respiration in the same cellular compartment. Some cyanobacteria can also fix atmospheric nitrogen alongside oxygenic photosynthesis and respiration. The redox components of these electron transport pathways are known to intersect in cyanobacteria. Majority of the energy-intensive processes occur in specialised membranes known as thylakoids. The coexistence of such remarkably complex metabolic pathways in a single cyanobacterial cell provides them with the potential to thrive in a wide variety of ecosystems. This metabolic complexity has sparked significant interest towards cyanobacterial research for the production of various high-value compounds with applications in the food, feed and fuel industry.

eLS subject area: Microbiology How to cite: Nagarajan, Aparna and Pakrasi, Himadri B (June 2016) Membrane-Bound Protein Complexes for Photosynthesis and Respiration in Cyanobacteria. In: eLS. John Wiley & Sons, Ltd: Chichester. DOI: 10.1002/9780470015902.a0001670.pub2

Introduction Cyanobacteria, previously known as blue green algae, are microbes with ancient lineage. Microfossils and stromatolites found 3.5 billion years ago (BYA) in Australia have suggested the presence of oxygen-evolving organisms, presumably cyanobacteria (Schopf, 2010). With their ability for oxygenic photosynthesis these organisms are believed to have evolved prior to 2.4 BYA to generate enough molecular oxygen to accumulate in the atmosphere (Buick, 2008). They are the only group of photosynthetic bacteria with the metabolic capabilities of converting light into cellular fuel and producing molecular oxygen as a byproduct. They also utilise the sugars to convert to CO2 and release energy during respiration. The intrinsic ability to carry out complex electron transfer pathways such as photosynthesis and respiration in a single cell compartment imparts special interest to this group of organisms. Certain species of cyanobacteria can also fix nitrogen (from N2 to NH3 ) using a specialised oxygen-sensitive enzyme called nitrogenase (Welsh et al., 2008). The combination of these processes makes them metabolically flexible and remarkably robust to thrive in environments ranging from freshwater, marine and terrestrial ecosystems to extreme environments such as hot springs and deserts (Bryant, 1994). See also: Cyanobacteria; Nitrogen Fixation in Cyanobacteria As gram-negative bacteria, the cell envelope of cyanobacteria consists of the outer membrane, peptidoglycan layer and plasma membrane. In addition, these organisms also have an internal membrane system, thylakoids, that separates the cytoplasm from the lumen and contains both photosynthetic and respiratory machinery. These electron transfer pathways intersect and share certain redox-active components described in later sections. Figure 1 provides a schematic representation of the membrane systems in cyanobacteria. The only oxygenic photosynthetic cyanobacterium devoid of thylakoids belongs to the genus Gloeobacter. These organisms host the photosynthetic

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Membrane-Bound Protein Complexes for Photosynthesis and Respiration in Cyanobacteria

Outer membrane Peptidoglycan layer

Plasma membrane

Membrane bound complexes involved in photosynthesis and respiration Thylakoid membrane NDH

PSII

Cyt b6f

PSI

Ox

ATP synthase

Lumen

Figure 1 Schematic representation of a cyanobacterial cell highlighting the membrane bound complexes involved in photosynthesis and respiration localised in specialised thylakoid membranes – the powerhouse of oxygenic photosynthetic organisms.

and respiratory machinery in the plasma membrane. This unique characteristic may be indicative of an early divergence of Gloeobacter placing them at the earliest branch of the cyanobacterial phylogenetic tree. In plant chloroplasts, thylakoids are organised to form an intrinsic network of interconnected stacked grana and unstacked stroma. However, cyanobacteria do not form such stacked and unstacked regions. Instead, thylakoid membranes in some cyanobacteria such as Synechocystis sp. PCC 6803 and Synechococus elongatus 7942 form concentric layers and follow the shape of the cell (Meene et al., 2005). In other cyanobacteria (for example Cyanothece sp. PCC 51142), thylakoid membranes form a dense network that extends throughout the cell (Liberton et al., 2011). See also: Plant Chloroplasts and Other Plastids Photosynthesis can be divided into light absorption and energy transfer by antenna systems, electron transfer and energy stabilisation in reaction centres and synthesis of high-energy molecules. Accordingly, the photosynthetic apparatus in cyanobacteria consists of soluble light harvesting antenna called phycobilisomes (PBS), and membrane protein complexes photosystem II (PSII), cytochrome b6 f (Cyt b6 f), photosystem I (PSI) and adenosine triphosphate (ATP) synthase (Figure 1). Photosynthetic pigments play a crucial role in light absorption and the energy delivery process. These primarily include chlorophylls, bilins and carotenoids. Different photosynthetic organisms differ in their pigment composition and distribution. See also: Plant Chloroplasts and Other Plastids 2

Energy Transfer by Antenna Complexes PBS are the light-harvesting antenna complexes in cyanobacteria that function in absorbing light and transferring to the reaction centre (MacColl, 1998). Pigmented phycobiliproteins and non-pigmented linker proteins assemble into massive PBS attached to the stromal side of thylakoid membranes. Phycobiliproteins contain covalently attached bilin chromophores that are primarily involved in light absorption and energy transfer. Cyanobacteria are known to regulate the structure and composition of PBS in response to changes in light and nutrient availability (Grossman et al., 1993). Structurally, PBS can be divided into a central core and peripheral rods to form a fan-shaped structure (Figure 2). The bilins in the rods and core often differ in their spectral properties to allow energy transfer from higher energy blue absorbing pigments in PBS to lower energy pigments in the reaction centre. PBS are primarily involved in delivering energy to PSII for photochemistry. However, recent studies have isolated and characterised a megacomplex of PBS with both PSII and PSI, indicating the association of PBS with both the reaction centres (Liu et al., 2013). In addition to PBS, cyanobacteria also have integral membrane antenna proteins such as CP43 and CP47 in PSII and energy is delivered from PBS to these proteins.



Light

PBS

NADP NAD(P)H

NAD(P)H

SDH

NADP

Fdox

O2

FdredH2O

+

O2 + H

PQ

CO2

NDH-1

2H2O

PSII

ATP

Cyt b6f

O2

ADP

PC

COX

PSI

Lumen

ATP Synthase

Cytoplasm PQ PC PQ P PC PC PQ

PC

PQ

PQ PC PC

PQ

Figure 2 Diagrammatic representation of the photosynthetic and respiratory electron transport chain components embedded in the thylakoid membranes of a cyanobacterial cell. Electron transfer reactions are highlighted in red.

Reaction Centres and Photosynthetic Electron Transport Photosystem II PSII is the reaction centre that undergoes water oxidation to produce molecular oxygen. It is the only biological system known that is capable of catalysing this crucial and thermodynamically difficult process. Structurally, PSII is a dimeric multisubunit membrane protein complex with each monomer consisting of more than 20 protein subunits and several cofactors such as chlorophylls, pheophytins, quinones, calcium, chloride, manganese atoms and nonhaem iron. Remarkable progress has been made towards resolving the three-dimensional (3D) crystal structure of PSII, enabling an improved understanding on the mechanism of PSII (Zouni et al., 2001; Umena et al., 2011). The core intrinsic subunits of PSII – D1, D2, CP43 and CP47 are essentially conserved in all oxygenic photosynthetic organisms (Table 1). D1 and D2 bind cofactors including P680, a special pair chlorophyll necessary for the primary photochemistry to generate sufficient oxidising power that drives water oxidation (Vinyard et al., 2013). CP43 and CP47 are core chlorophyll-binding antenna proteins that funnel energy to P680 in D1. The catalytic centre of PSII that performs the

water-splitting process is a tetranuclear Mn4 CaO5 cluster called the oxygen-evolving complex (OEC), located on the lumenal face of PSII. There are other extrinsic protein subunits such as PsbO, PsbV, PsbU, PsbQ and PsbP that are crucial for maintaining the stability of the OEC (Bricker et al., 2012; Roose et al., 2016). The assembly and life cycle of PSII is an area of active research, and for recent advances refer to Nickelsen and Rengstl (2013). See also: Photosystem II; Photosynthesis

Photosystem I PSI is the reaction centre that catalyses oxidation of plastocyanin (PC) and reduction of Ferredoxin (Fd) to generate ATP and NAD(P)H. Cyanobacterial PSI functions as a trimer, the crystal structure of which has been determined (Jordan et al., 2001). Each monomer consists of 12 protein subunits and 129 cofactors including chlorophylls, iron–sulfur (Fe-S) clusters, beta-carotene, phylloquinones and lipids. The core of PSI is a heterodimeric complex of protein subunits PsaA and PsaB that provide the binding site for P700, a special pair chlorophyll (Table 1). A unique feature of PSI is the set of three iron–sulfur (Fe-S) clusters that function as early electron acceptors. Other accessory proteins have also been identified that predominantly function as assembly factors and are essential for stable accumulation of PSI in the cell (Yang et al., 2015). See also: Photosystem I


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Table 1 Major thylakoid membrane bound complexes involved in photosynthesis and respiration in cyanobacteria Complex

Major subunits

Cofactors

Function

Photosystem II

Core: D1, D2, CP43 and CP47 Extrinsic: PsbO, PsbU, PsbV, PsbP, PsbQ Core: PsaA, PsaB Other: PsaC-F, PsaI-M, PsaX OPS domain: NdhL-Q, NdhS

Mn, Ca, Cl, O, Fe, PQ, Chl, pheophytin

Light-induced water oxidation and reduction of PQ

Chl, Fe-S centers, phylloquinones, beta-carotene Fe-S centers

SdhA, SdhB, SdhC

Flavin, Fe-S centers

Redox active: cyt b6 , cyt f, Rieske protein Non-Redox: Subunit IV CtaC, CtaD, CtaE

2 cyt b, cyt f (cyt c), Fe-S

Light-induced oxidation of PC/cyt c553 and reduction of Fd NAD(P)H oxidation and PQ reduction Succinate oxidation and PQ reduction PQH2 oxidation and PC/cyt c553 reduction

Photosystem I Type I – NAD(P)H dehydrogenase Succinate dehydrogenase Cytochrome b6 f

Cytochrome oxidase

CuA , CuB , Mg, cyt a, cyt a3

PSI is one of the most efficient photoelectric apparatus in nature wherein every photon received by PSI is used for electron translocation with a quantum efficiency of nearly 100% (Nelson and Yocum, 2006). PSI contributes in both linear and cyclic electron flow (CEF) and plays an important role in photosynthetic acclimation to changing environment mainly by participating in CEF and adjustment of PS stoichiometry. Technological advances have enabled the evaluation of CEF experimentally and indicated a larger percentage contribution of CEF than previously predicted (Kramer and Evans, 2011). Recent studies also provide evidence for the involvement of CEF for acclimation in fluctuating light (Suorsa et al., 2012) and cold stress (Berla et al., 2015). In CEF, electrons flow only through PSI/Fd to PQ (plastoquinone) and Cyt b6 f back to PSI again in a cyclic manner (Bendall and Manasse, 1995). This electron transfer pathway contributes to a proton gradient used for ATP synthesis but does not involve PSII and results in no net NADP+ reduction. The PSI to PSII ratio in most higher plants is 1 owing to an equal amount of PSI and PSII, whereas in some species of cyanobacteria this ratio is much larger than 1 possibly because of involvement of PSI in CEF. The high amount of PSI may serve to compete with cytochrome oxidase (COX) for electrons, thus maximising the number of electrons for CO2 fixation.

Photosynthetic electron flow Electrons generated from the light-driven oxidation of P680 are used to reduce the PQ pool and transferred to the Cyt b6 f complex. Electrons from Cyt b6 f are next transferred to a soluble electron carrier PC (copper containing enzyme) or cytochrome c553 depending on the species and availability of copper. The soluble one-electron carrier reduces the oxidised PSI reaction centre chlorophyll P700+ . PSI oxidation occurs with the light-driven transfer of electron to Fd and eventually to NADP to form NADPH (Figure 2). In cyanobacteria, some components of the electron transport pathways are shared between photosynthesis and respiration. These include the PQ pool, Cyt b6 f and soluble electron carriers such as PC and c553 . 4

Cyt c oxidation and O2 reduction

Respiratory Electron Transport Respiration in cyanobacteria serves to maintain a proton gradient across the thylakoid membrane wherein both the photosynthetic and respiratory electron transport chains intersect. These processes are carefully regulated to maintain the redox poise of all the components of the electron transport pathways and prevent oxidative damage. Cyanobacterial respiration is diverse, and several alternative electron donors and oxidases exist, the contributions of which remain unclear. The main components of respiratory electron transfer process are NAD(P)H dehydrogenase (NDH-1), succinate dehydrogenase (SDH), Cyt b6 f and COX as well as other terminal oxidases. Studies using mutants lacking specific respiratory proteins in Synechocystis sp. PCC 6803 have shown that SDH (Complex II) is more important in donating electrons to the PQ pool during respiration rather than the NDH-1 (Complex I) (Cooley et al., 2000). Both NDH-1 and SDH are detected exclusively in thylakoid membranes (Liu et al., 2012). In addition to Cyt b6 f (Schultze et al., 2009), COX is localised in thylakoid membranes (Howitt and Vermaas, 1998). See also: Photorespiration; Photosynthetic Carbon Metabolism

NAD(P)H dehydrogenase (NDH-1) The NDH-1 complex preferentially accepts electrons from Fd, reduced by PSI, via CEF (Ohkawa et al., 2000). Over the last decade, considerable progress has been made in understanding the structure–function relationship of various subunits in the NDH-1 complex. Reverse genetics and proteomics approaches have indicated the presence of three major NDH-1 complexes in cyanobacteria – large (NDH-1L), medium (NDH-1M) and small (NDH-1S) complex. Electron microscopic studies in cyanobacteria have revealed seven specialised NDH-1 subunits, NdhL, NdhM, NdhN, NdhO, NdhP, NdhQ and NdhS comprising of the oxygenic photosynthesis-specific (OPS) domain (Battchikova et al., 2011). Apart from NdhQ six other OPS subunits are found in higher plants but absent in Escherichia coli (E. coli). The structure and composition of NDH-1L is similar to that of the chloroplast and E. coli (Ogawa and Mi, 2007). On the



basis of several studies, the localisation and function of most of these subunits have been elucidated and extensively reviewed in Ma and Ogawa (2015). NDH-1L complexes are involved in respiration and the NDH-1M is involved in CO2 uptake, while all types of complexes participate in NDH-1-dependent CEF through PSI (Bernát et al., 2011). NDH-1-dependent CEF increases the proton gradient and supplies additional ATP for CO2 fixation, especially under environmental stress conditions such as high light (Endo et al., 1999) and heat (Ma and Mi, 2008). Synechocystis sp. PCC 6803 is capable of producing type-2 NDH (NDH-2), which is a single-subunit protein that may not contribute to a proton gradient across thylakoid membranes. NDH-2 is probably localised in the plasma membrane and might be involved in electron transfer reactions involving the quinol oxidase ARTO (Lea-Smith et al., 2013).

Succinate dehydrogenase (SDH) The presence of a functional SDH in cyanobacteria was established by identifying two of its components that are involved in succinate:quinol oxidoreductase activity. Deletion of these genes in Synechocystis sp. PCC 6803 resulted in a phenotype consistent with a lack of SDH activity (Cooley et al., 2000). While fumarate (the SDH product) is depleted in mutants lacking SDH, succinate accumulates. Cyanobacteria can convert 2-oxoglutarate to succinate even though traditional 2-oxoglutarate dehydrogenase is absent according to the genome sequence. Recent studies have identified two genes that functionally replace the enzyme activities of 2-oxoglutarate dehydrogenase and succinyl-CoA synthetase required to convert 2-oxoglutarate to succinate in the citric acid cycle (TCA (tricarboxylic acid) cycle). Both in vitro and in vivo studies have established the presence of a modified closed citric acid cycle in cyanobacteria contrary to the 50-year-long held belief of an incomplete TCA cycle (Zhang and Bryant, 2011; You et al., 2014). See also: Citric Acid Cycle

Terminal oxidases Most respiratory terminal oxidases belong to the haem–copper superfamily characterised with a CuB centre electronically coupled with a high spin haem. They reduce molecular oxygen to water and couple electron transfer with proton translocation across the membrane for ATP production. Depending on the nature of electron donors they are divided into COX (cytochrome c oxidase; aa3 type COXs) or quinol oxidases such as bo-type quinol oxidases. The bd-quinol oxidases are a different class of terminal oxidases that do not belong to the haem–copper superfamily since they lack the binuclear centre and instead have two haem groups and lack the capability of pumping protons (Hart et al., 2005). The main type of terminal oxidase in cyanobacteria is the aa3 type cytochrome c oxidase (COX) that is found to be localised in both in the thylakoid membrane and the plasma membrane (Peschek et al., 1994). The bd-type quinol oxidase could be demonstrated on the basis of inhibitor studies as well as by mutant analysis, but the bo-type oxidase does not appear to be expressed under the conditions used thus far in cyanobacteria.

The presence of COX in the cyanobacterial thylakoid membrane raises the question of what the electron donor may be. If cytochrome c553 , the luminal electron carrier that can replace PC, is present, then this is the likely electron donor. However, electron transfer to the oxidase can also occur in the absence of c553 and probably involves PC and another cytochrome, cM . This cytochrome cM may serve as an electron transport intermediate and might be associated with the COX complex. Cytochrome cM appears to be required for electron flow out of the PQ pool under conditions that PSI and cytochrome c553 are absent (Manna and Vermaas, 1997). See also: Cytochrome c Oxidase

Components Shared between Photosynthesis and Respiration The plastoquinone (PQ) pool PQ pool is a lipophilic membrane-bound carrier in the thylakoid membrane that shuttles electrons from both photosynthetic and respiratory electron transport chains to the Cyt b6 f complex. Electrons extracted from water are transferred through the primary quinone acceptor QA in the stromal side of PSII. The electron is further transferred to a PQ molecule in the secondary quinone acceptor QB of PSII, to form a semiquinone that is stable for several seconds and subsequently reduced to plastoquinol (PQH2 ). PQH2 is formed by accepting two reducing equivalents and equilibrates with the PQ pool in the thylakoid membrane. Therefore, PQ can function as an adapter converting one-electron redox reactions to two-electron reactions and vice versa. See also: Quinone Cofactors

Cytochrome b6 f (Cyt b6 f ) A key complex in both photosynthetic and respiratory electron transfer in cyanobacteria is the Cyt b6 f complex. They function as oligomeric quinol cytochrome c/PC oxidoreductases capable of proton translocation across the thylakoid membrane. Cyt b6 f functions as a homodimer with each monomer comprising of eight subunits with four components including the redox-active components cytochrome b6 , the cytochrome f, and the Rieske-type 2Fe-2S protein. A fourth major component, subunit IV, does not carry redox-active cofactors. The Cyt b6 f complex is in many respects analogous to the cytochrome bc1 complex in mitochondria and gram-negative bacteria. The cytochrome b of bc1 complex corresponds to cytochrome b6 and subunit IV. Another interesting feature when comparing cytochrome b6 f and cytochrome bc1 complexes is that cytochrome f and cytochrome c1 do not have a common ancestor, in spite of their homologous function. See also: Mitochondria: Structure and Role in Respiration Cyt b6 f plays a central role in generating a proton gradient for ATP synthesis via the redox loop Q-cycle to maintain the ATP/NAD(P)H ratio for CO2 fixation. The two-electron oxidation of plastoquinol (PQH2 ) occurs via a split pathway wherein one electron is donated to the Rieske-type 2Fe-2S protein, which is the electron donor to cytochrome f ultimately transferring


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one of the two electrons to PSI via PC; the other electron is donated to the lower potential cytochrome b haems (Cramer and Zhang, 2006). An interesting feature of the cyanobacterial Cyt b6 f complex is the presence of multiple copies of petC genes that code for Rieske 2Fe-2S centres. This multiplicity enables adaptation to stress conditions such as fluctuating light intensities (Tsunoyama et al., 2009) and low oxygen (Summerfield et al., 2008). See also: Iron Cofactors: Nonhaem

Soluble electron carriers Both PC and cytochrome c553 , otherwise known as cytochrome c6, are soluble metalloproteins that act as alternative electron carriers between Cyt b6 f and PSI and function in both photosynthesis and respiration. PC and cytochrome c553 differ in the nature of their redox centres wherein one is a copper protein and the other is a haem protein respectively. These soluble electron carriers are often exchangeable and studies in Synechocystis sp. PCC 6803 have shown a copper-mediated regulation for the expression of the electron carriers (Zhang et al., 1992). In mutants lacking either PC or cytochrome c553 , photosynthetic electron transport rates remain normal, indicating that either of the two soluble carriers is sufficient. Interestingly, efforts to delete the genes for both PC and cytochrome c553 in the same strain have been unsuccessful, indicating that one of the two carriers is required to shuttle electrons to PSI and COX.

ATP synthase The ATP required for CO2 fixation is produced by the F1-F0- ATP synthase that utilises the proton motive force (pmf) generated across the thylakoid membrane to catalyse the formation of ATP from ADP. F1 is the membrane extrinsic catalytic domain of the ATP synthase, composed of five different subunits (𝛼-𝜀). F0 is composed of four different subunits (b, b′ , c and a) and forms the membrane intrinsic portion of ATP synthase (von Ballmoos et al., 2009). Majority of pmf generated across thylakoid membranes is from the ΔpH component contrary to respiratory chains in bacteria and mitochondria wherein it is stored as electric field. A lumen pH value below 6.5 slows down plastoquinol reoxidation at the Cyt b6 f to rebalance the consumption of the pmf by ATP synthase (Kramer et al., 1999).

Regulation of Photosynthesis and Respiration Regulation of photosynthesis and respiration is very important for allowing cyanobacteria to thrive in diverse environmental conditions. Light-driven electron transport reactions during photosynthesis often lead to the production of reactive oxygen species that cause oxidative damage in the cell. This phenomenon is called photoinhibition, caused primarily by the high light, and is an area of extensive research. To cope with stress conditions, cyanobacteria have evolved several mechanisms such as the structure–function plasticity of PBS and damage–repair cycle of PSII. PBS complexes can sense and respond to changes in the environment such as changes in light or nutrient availability either by changing pigment composition or by degrading PBS to prevent photoinhibition (Grossman et al., 1993). Cyanobacteria also express specialised integral antenna proteins such as IsiA during stress conditions such as iron starvation for light harvesting (Singh and Sherman, 2007). Oxygenic photosynthetic organisms have developed a complex repair cycle of PSII wherein damage to PSII, in particular the D1 subunit, is sensed and degraded by FtsH protease. The damage and repair cycle of PSII is complex wherein PSII first undergoes disassembly to allow for the replacement of damaged D1 (buried within PSII) with newly synthesised D1 and this is followed by reassembly of PSII. The rate and capacity of the various steps is an important aspect of regulation. The approximate capacities of electron transfer steps in Synechocystis sp. PCC 6803 are summarised in Table 2 (Vermaas, 2001). The actual rate of reactions may be significantly lower in vivo, depending on the conditions (light intensity, redox state, etc.). From Table 2 it is clear that PS I activity is abundant relative to that of the Cyt b6 f complex, and this may explain in part the slow P700+ rereduction kinetics that are generally observed after a period of illumination. If light is abundant, the photosynthetic electron transport chain has a much higher capacity of electron flow than the respiratory chain, but at lower light intensity or in darkness respiratory rates are higher. As the capacities of COX and SDH seem comparable, respiratory electron flow will not lead to major changes in the redox state of the PQ pool, leaving room for regulation of metabolic processes that are apparently mediated via the PQ redox state. See also: Photosynthesis: Light Reactions

Table 2 Approximate capacity and probable source of rate limitation of photosynthetic and respiratory electron transfer in Synechocystis sp. PCC 6803 Complex

Capacity (μmol electrons h−1 (mg Chl)−1 )

Source of rate limitation

Photosystem II Photosystem I Type I – NAD(P)H dehydrogenase Succinate dehydrogenase Cytochrome b6 f Cytochrome oxidase

1000 3000 20 200 1000 200

Light intensity and availability of oxidised PQ Light intensity, Fd/NADP availability, reduced cyt c553 /PC NAD(P)H availability, PQ pool redox state Succinate concentration, PQ pool redox state PQH2 concentration Reduced cyt c553 /PC availability

For simplicity, these values have been expressed on a per-chlorophyll basis.

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Acknowledgements The studies at Washington University were supported by the U.S. Department of Energy, Office of Science, Basic Energy Sciences, under Award # DE-FG02-99ER20350 to HBP. We thank the Pakrasi lab members for helpful collegial discussions that benefited the development of this chapter.

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Further Reading Blankenship RE (2014) Molecular Mechanisms of Photosynthesis. Oxford, UK: Wiley-Blackwell. Liberton M and Pakrasi HB (2008) Membrane systems in cyanobacteria. In: Herrero A and Flores E (eds) The Cyanobacteria: Molecular Biology, Genomics, and Evolution, pp. 217–287. Norwich, UK: Horizon Scientific Press. Nixon PJ, Michoux F, Yu J, Boehm M and Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Annals of Botany 106: 1–16. Ort DR, Yocum CF and Heichel IF (1996) Oxygenic Photosynthesis: The Light Reactions. Netherlands: Kluwer Academic Publishers. Schmetterer G (2004) Cyanobacterial respiration. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp. 409–435. Dordrecht: Springer. Yoshioka-Nishimura M and Yamamoto Y (2014) Quality control of Photosystem II: the molecular basis for the action of FtsH protease and the dynamics of the thylakoid membranes. Journal of Photochemistry and Photobiology B: Biology 137: 100–106.
