Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

Schuller, Jan M.; Saura, Patricia; Thiemann, Jacqueline; Schuller, Sandra K.; Gámiz‐Hernández, Ana P.; Kurisu, Genji; Nowaczyk, Marc M.; Kaila, Ville R. I.

doi:10.1038/s41467-020-14347-4

Cited by 64 publications

(71 citation statements)

References 71 publications

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“…Moreover complemented mutants with inactive γCA variants is sufficient to complement the mutant phenotype, showing that carbonic anhydrase activity is not essential 20 . Recently it was shown that carbonic anhydrase activity is also present in photosynthetic cyanobacterial complex I, but is carried out by a different type of CA enzyme, positioned at the end of the P D module that would contribute to proton generation 24 . However, in plant mitochondrial complex I, the only conserved active site is positioned at the most distal position relative to the membrane.…”

Section: Resultsmentioning

confidence: 99%

Specific features and assembly of the plant mitochondrial complex I revealed by cryo-EM

Soufari¹,

Parrot²,

Kuhn³

et al. 2020

Nat Commun

119

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Mitochondria are the powerhouses of eukaryotic cells and the site of essential metabolic reactions. Complex I or NADH:ubiquinone oxidoreductase is the main entry site for electrons into the mitochondrial respiratory chain and constitutes the largest of the respiratory complexes. Its structure and composition vary across eukaryote species. However, high resolution structures are available only for one group of eukaryotes, opisthokonts. In plants, only biochemical studies were carried out, already hinting at the peculiar composition of complex I in the green lineage. Here, we report several cryo-electron microscopy structures of the plant mitochondrial complex I. We describe the structure and composition of the plant respiratory complex I, including the ancestral mitochondrial domain composed of the carbonic anhydrase. We show that the carbonic anhydrase is a heterotrimeric complex with only one conserved active site. This domain is crucial for the overall stability of complex I as well as a peculiar lipid complex composed of cardiolipin and phosphatidylinositols. Moreover, we also describe the structure of one of the plant-specific complex I assembly intermediates, lacking the whole PD module, in presence of the maturation factor GLDH. GLDH prevents the binding of the plant specific P1 protein, responsible for the linkage of the PP to the PD module.

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Section: Resultsmentioning

confidence: 99%

Specific features and assembly of the plant mitochondrial complex I revealed by cryo-EM

Soufari¹,

Parrot²,

Kuhn³

et al. 2020

Nat Commun

119

View full text Add to dashboard Cite

show abstract

“…Moreover complemented mutants with inactive γCA variants is sufficient to complement the mutant phenotype, showing that carbonic anhydrase activity is not essential 19 . Recently it was shown that carbonic anhydrase activity is also present in photosynthetic complex I, but is carried out by a different type of CA enzyme, positioned at the end of the PD module that would contribute to proton generation 21 . However, in our complex, the only conserved active site is positioned at the most distal position relative to the membrane.…”

Section: Carbonic Anhydrase: Specific Component Of the Plant Complex Imentioning

confidence: 99%

Specific features and assembly of the plant mitochondrial complex I revealed by cryo-EM

Soufari

Parrot

Kuhn

et al. 2020

Preprint

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Mitochondria are the powerhouses of eukaryotic cells and the site of essential metabolic reactions. Their main purpose is to maintain the high ATP/ADP ratio that is required to fuel the countless biochemical reactions taking place in eukaryotic cells 1 . This high ATP/ADP ratio is maintained through oxidative phosphorylation (OXPHOS). Complex I or NADH:ubiquinone oxidoreductase is the main entry site for electrons into the mitochondrial respiratory chain and constitutes the largest of the respiratory complexes 2 . Its structure and composition varies across eukaryotes species. However, high resolution structures are available only for one group of eukaryotes, opisthokonts 3-6 . In plants, only biochemical studies were carried out, already hinting the peculiar composition of complex I in the green lineage. Here, we report several cryoelectron microscopy structures of the plant mitochondrial complex I at near-atomic resolution. We describe the structure and composition of the plant complex I including the plant-specific additional domain composed by carbonic anhydrase proteins. We show that the carbonic anhydrase is an heterotrimeric complex with only one conserved active site. This domain is crucial for the overall stability of complex I as well as a peculiar lipid complex composed cardiolipin and phosphatidylinositols. Moreover we also describe the structure of one of the plant-specific complex I assembly intermediate, lacking the whole PD module, in presence of the maturation factor GLDH. GLDH prevents the binding of the plant specific P1 protein, responsible for the linkage of the PP to the PD module. Finally, as the carbonic anhydrase domain is likely to be associated with complex I from numerous other known eukaryotes, we propose that our structure unveils an ancestral-like organization of mitochondrial complex I.Complex I is the largest multimeric enzyme of the respiratory chain, composed of more than 40 protein subunits. 14 are strictly conserved proteins subunits, vestige of complex I of bacterial origin 7 . The additional subunits, referred to as supernumerary subunits, were acquired during eukaryotes evolution. Part of these additional subunits are conserved among other eukaryotes and play essential roles for the structure, function and the association with the other respiratory chain complexes, eg. to assemble into respirasome in animals 8 . Recently, several high resolution 3D structures of the complete mitochondrial complex I of opisthokonts were determined by cryo-EM in mammalian species 4-6 and in the aerobic yeast Yarrowia lipolytica 3,9 , revealing the organization of their additional specie-specific subunits. However, in plants, even though extensive biochemical characterization was conducted 10,11 , high-resolution structures of mitochondrial complex I are yet to be derived. Early negative staining studies 12 revealed the presence of a large additional membrane attached domain, absent from animal and yeast species, hinting at the peculiar structure and composition of the plant complex I.In order...

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“…NADH dehydrogenase complex I, or complex I, is a widely distributed bioenergetic complex, with homologs seen in archaea, bacteria, and eukaryotes [1]. The core structure of these complexes and their subunit composition have been largely conserved throughout these phyletic kingdoms, with the bacterial complexes possessing the fewest subunits, and eukaryotes possessing accessory subunits, but retaining a core that is conserved across the domains of life [2][3][4][5][6][7]. These complexes are vital parts of a diverse variety of electron transport chains and have been shown to couple proton pumping to electron transport from ferredoxin (Fd) or NAD(P)H to a quinone to increase the proton motive force (PMF) for ATP production in heterotrophic bacteria as well as mitochondria and chloroplasts [3,[8][9][10][11][12][13].…”

Section: Introductionmentioning

confidence: 99%

“…Cyanobacteria also possess complex I, however they are unique in possessing four functional versions of complex I, and they are termed NDH-1 for NADPH Dehydrogenase 1 complex, though they have recently been shown to utilize Fd for their reductant over NADPH [7,19,20]. Recently, the structure of two cyanobacterial NDH-1 complexes have been solved [4][5][6][7], covering representatives of the major functions of these complexes: Cyclic electron flow (CEF), respiratory electron flow, and CO2 uptake. A summary of the components of photosynthetic electron flow, their actions on proton pumping, and inhibitors utilized here are shown in Fig.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Electron flow through NDH-1 complexes is the major driver of cyclic electron flow-dependent proton pumping in cyanobacteria

Miller

Vaughn²,

Burnap

2020

Preprint

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Cyclic electron flow (CEF) around Photosystem I is vital to balancing the photosynthetic energy budget of cyanobacteria and other photosynthetic organisms. The coupling of CEF to proton pumping has long been hypothesized to occur, providing proton motive force (PMF) for the synthesis of ATP with no net cost to [NADPH]. This is thought to occur largely through the activity of NDH-1 complexes, of which cyanobacteria have four with different activities. While a much work has been done to understand the steady-state PMF in both the light and dark, and fluorescent probes have been developed to observe these fluxes in vivo, little has been done to understand the kinetics of these fluxes, particularly with regard to NDH-1 complexes. To monitor the kinetics of proton pumping in Synechocystis sp. PCC 6803, the pH sensitive dye Acridine Orange was used alongside a suite of inhibitors in order to observe light-dependent proton pumping. The assay was demonstrated to measure photosynthetically driven proton pumping and used to measure the rates of proton pumping unimpeded by dark ΔpH. Here, the cyanobacterial NDH-1 complexes are shown to pump a sizable portion of proton flux when CEF-driven and LEF-driven proton pumping rates are observed and compared in mutants lacking some or all NDH-1 complexes. It is also demonstrated that PSII and LEF are responsible for the bulk of light induced proton pumping, though CEF and NDH-1 are capable of generating ~40% of the proton pumping rate when LEF is inactivated.

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Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

Cited by 64 publications

References 71 publications

Specific features and assembly of the plant mitochondrial complex I revealed by cryo-EM

Specific features and assembly of the plant mitochondrial complex I revealed by cryo-EM

Specific features and assembly of the plant mitochondrial complex I revealed by cryo-EM

Electron flow through NDH-1 complexes is the major driver of cyclic electron flow-dependent proton pumping in cyanobacteria

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