Probing the electric field across thylakoid membranes in cyanobacteria

Viola, Stefania; Bailleul, Benjamin; Yu, Jianfeng; Nixon, Peter J.; Sellés, Julien; Joliot, Pierre; Wollman, Françis-André

doi:10.1073/pnas.1913099116

Cited by 20 publications

(36 citation statements)

References 48 publications

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“…To inspect whether the phenotypes observed above depend on differential build‐up or regulation of pmf , we measured in vivo changes in the pmf by monitoring the absorbance change difference between 500 and 480 nm, which constitutes the electrochromic shift (ECS) in Synechocystis (Viola et al ., 2019). In vivo measurement of light‐induced ECS revealed that after 1 sec of illumination of dark‐adapted WT cells with 500 μmol photons m −2 sec −1 , high pmf level was transiently generated, followed by decline during the subsequent seconds (Figure 5e).…”

Section: Resultsmentioning

confidence: 99%

“…In both Δ flv3 and Δ flv3 d1d2 , pmf and thylakoid proton flux (vH+) were lower than in WT after 1 sec (Figure 5g). In Δ flv3 , pmf remained drastically lower than in WT during the first seconds of illumination, but differed only slightly from WT thereafter due to diminished conductivity of the thylakoid membrane (gH+) (Figure 5f), which is mainly determined by the activity of the adenosine triphosphate (ATP) synthase (Cruz et al ., 2005; Viola et al ., 2019). In ∆ d1d2 , the thylakoid proton flux was similar to WT (Figure 5g), probably due to enhanced FDP activity (Figure 2c) compensating for impaired CET and respiration.…”

Section: Resultsmentioning

confidence: 99%

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Functional redundancy between flavodiiron proteins and NDH‐1 in Synechocystis sp. PCC 6803

et al. 2020

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Summary In oxygenic photosynthetic organisms, excluding angiosperms, flavodiiron proteins (FDPs) catalyze light‐dependent reduction of O2 to H2O. This alleviates electron pressure on the photosynthetic apparatus and protects it from photodamage. In Synechocystis sp. PCC 6803, four FDP isoforms function as hetero‐oligomers of Flv1 and Flv3 and/or Flv2 and Flv4. An alternative electron transport pathway mediated by the NAD(P)H dehydrogenase‐like complex (NDH‐1) also contributes to redox hemostasis and the photoprotection of photosynthesis. Four NDH‐1 types have been characterized in cyanobacteria: NDH‐11 and NDH‐12, which function in respiration; and NDH‐13 and NDH‐14, which function in CO2 uptake. All four types are involved in cyclic electron transport. Along with single FDP mutants (∆flv1 and Δflv3) and the double NDH‐1 mutants (∆d1d2, which is deficient in NDH‐11,2 and ∆d3d4, which is deficient in NDH‐13,4), we studied triple mutants lacking one of Flv1 or Flv3, and NDH‐11,2 or NDH‐13,4. We show that the presence of either Flv1/3 or NDH‐11,2, but not NDH‐13,4, is indispensable for survival during changes in growth conditions from high CO2/moderate light to low CO2/high light. Our results show functional redundancy between FDPs and NDH‐11,2 under the studied conditions. We suggest that ferredoxin probably functions as a primary electron donor to both Flv1/3 and NDH‐11,2, allowing their functions to be dynamically coordinated for efficient oxidation of photosystem I and for photoprotection under variable CO2 and light availability.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Functional redundancy between flavodiiron proteins and NDH‐1 in Synechocystis sp. PCC 6803

et al. 2020

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“…This conclusion was consistent with the results of mutant analyses ( Figure 5 and Figure 6 ) and is in agreement with the fact that the electron sink capacity of the alternative electron transport from PSII to respiratory terminal oxidases is not significant in light, compared with photosynthetic linear electron flow and FLV-mediated electron transports [ 36 , 45 ]. Based on the present dataset, we cannot exclude the possibility that the LER measured after the actinic light was turned off did not necessarily reflect the exact respiratory O 2 uptake during illumination since the membrane potential, also called proton motive force , depends on both the respiratory and photosynthetic electron transport chains in the thylakoid membrane [ 46 ], which possibly suppresses the respiratory electron transport via “back-pressure” of the proton motive force [ 47 ]. Meanwhile, the net O 2 evolution rate decreased with Y(II) being kept constant ( Figure 2 and Figure 3 ), supporting the hypothesis that LER exactly occurs during the illumination.…”

Section: Discussionmentioning

confidence: 99%

Characterization of Light-Enhanced Respiration in Cyanobacteria

Shimakawa

Kohara

Miyake

2020

IJMS

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In eukaryotic algae, respiratory O2 uptake is enhanced after illumination, which is called light-enhanced respiration (LER). It is likely stimulated by an increase in respiratory substrates produced during photosynthetic CO2 assimilation and function in keeping the metabolic and redox homeostasis in the light in eukaryotic cells, based on the interactions among the cytosol, chloroplasts, and mitochondria. Here, we first characterize LER in photosynthetic prokaryote cyanobacteria, in which respiration and photosynthesis share their metabolisms and electron transport chains in one cell. From the physiological analysis, the cyanobacterium Synechocystis sp. PCC 6803 performs LER, similar to eukaryotic algae, which shows a capacity comparable to the net photosynthetic O2 evolution rate. Although the respiratory and photosynthetic electron transports share the interchain, LER was uncoupled from photosynthetic electron transport. Mutant analyses demonstrated that LER is motivated by the substrates directly provided by photosynthetic CO2 assimilation, but not by glycogen. Further, the light-dependent activation of LER was observed even with exogenously added glucose, implying a regulatory mechanism for LER in addition to the substrate amounts. Finally, we discuss the physiological significance of the large capacity of LER in cyanobacteria and eukaryotic algae compared to those in plants that normally show less LER.

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“…The pmf composition and dynamics in cyanobacteria has not yet been well studied, whereas an electrochromic shift of carotenoid pigments in the thylakoid membranes of eukaryotes (Bailleul et al, 2010), has allowed focused studies primarily in the green lineage (Bailleul et al, 2015). The recent report of a useable electrochromic shift in a cyanobacterium should make such studies possible (Viola et al, 2019).…”

Section: Davis and Kramermentioning

confidence: 99%

Optimization of ATP Synthase c–Rings for Oxygenic Photosynthesis

Davis

Kramer

2020

Front. Plant Sci.

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The conversion of sunlight into useable cellular energy occurs via the proton-coupled electron transfer reactions of photosynthesis. Light is absorbed by photosynthetic pigments and transferred to photochemical reaction centers to initiate electron and proton transfer reactions to store energy in a redox gradient and an electrochemical proton gradient (proton motive force, pmf), composed of a concentration gradient (DpH) and an electric field (Dy), which drives the synthesis of ATP through the thylakoid F o F 1 -ATP synthase. Although ATP synthase structure and function are conserved across biological kingdoms, the number of membrane-embedded ion-binding c subunits varies between organisms, ranging from 8 to 17, theoretically altering the H + /ATP ratio for different ATP synthase complexes, with profound implications for the bioenergetic processes of cellular metabolism. Of the known c-ring stoichiometries, photosynthetic c-rings are among the largest identified stoichiometries, and it has been proposed that decreasing the c-stoichiometry could increase the energy conversion efficiency of photosynthesis. Indeed, there is strong evidence that the high H + /ATP of the chloroplast ATP synthase results in a low ATP/nicotinamide adenine dinucleotide phosphate (NADPH) ratio produced by photosynthetic linear electron flow, requiring secondary processes such as cyclic electron flow to support downstream metabolism. We hypothesize that the larger c subunit stoichiometry observed in photosynthetic ATP synthases was selected for because it allows the thylakoid to maintain pmf in a range where ATP synthesis is supported, but avoids excess Dy and DpH, both of which can lead to production of reactive oxygen species and subsequent photodamage. Numerical kinetic simulations of the energetics of chloroplast photosynthetic reactions with altered cring size predicts the energy storage of pmf and its effects on the photochemical reaction centers strongly support this hypothesis, suggesting that, despite the low efficiency and suboptimal ATP/NADPH ratio, a high H + /ATP is favored to avoid photodamage. This has important implications for the evolution and regulation of photosynthesis as well as for synthetic biology efforts to alter photosynthetic efficiency by engineering the ATP synthase.

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Probing the electric field across thylakoid membranes in cyanobacteria

Cited by 20 publications

References 48 publications

Functional redundancy between flavodiiron proteins and NDH‐1 in Synechocystis sp. PCC 6803

Functional redundancy between flavodiiron proteins and NDH‐1 in Synechocystis sp. PCC 6803

Characterization of Light-Enhanced Respiration in Cyanobacteria

Optimization of ATP Synthase c–Rings for Oxygenic Photosynthesis

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