The Complementary Roles of Chloroplast Cyclic Electron Transport and Mitochondrial Alternative Oxidase to Ensure Photosynthetic Performance

Chloroplasts use light energy and a linear electron transport (LET) pathway for the coupled generation of NADPH and ATP. It is widely accepted that the production ratio of ATP to NADPH is usually less than required to fulfill the energetic needs of the chloroplast. Left uncorrected, this would quickly result in an over-reduction of the stromal pyridine nucleotide pool (i.e., high NADPH/NADP+ ratio) and under-energization of the stromal adenine nucleotide pool (i.e., low ATP/ADP ratio). These imbalances could cause metabolic bottlenecks, as well as increased generation of damaging reactive oxygen species. Chloroplast cyclic electron transport (CET) and the chloroplast malate valve could each act to prevent stromal over-reduction, albeit in distinct ways. CET avoids the NADPH production associated with LET, while the malate valve consumes the NADPH associated with LET. CET could operate by one of two different pathways, depending upon the chloroplast ATP demand. The NADH dehydrogenase-like pathway yields a higher ATP return per electron flux than the pathway involving PROTON GRADIENT REGULATION5 (PGR5) and PGR5-LIKE PHOTOSYNTHETIC PHENOTYPE1 (PGRL1). Similarly, the malate valve could couple with one of two different mitochondrial electron transport pathways, depending upon the cytosolic ATP demand. The cytochrome pathway yields a higher ATP return per electron flux than the alternative oxidase (AOX) pathway. In both Arabidopsis thaliana and Chlamydomonas reinhardtii, PGR5/PGRL1 pathway mutants have increased amounts of AOX, suggesting complementary roles for these two lesser-ATP yielding mechanisms of preventing stromal over-reduction. These two pathways may become most relevant under environmental stress conditions that lower the ATP demands for carbon fixation and carbohydrate export.

Download Full-text

Phycobilisomes Harbor FNRL in Cyanobacteria

mBio ◽

10.1128/mbio.00669-19 ◽

2019 ◽

Vol 10 (2) ◽

Cited By ~ 9

Author(s):

Haijun Liu ◽

Daniel A. Weisz ◽

Mengru M. Zhang ◽

Ming Cheng ◽

Bojie Zhang ◽

...

Keyword(s):

Mass Spectrometry ◽

Energy Transfer ◽

Electron Transport ◽

Carbon Fixation ◽

Close Association ◽

Reaction Centers ◽

Light Energy ◽

Fine Tuning ◽

Cyclic Electron Transport ◽

Cross Link

ABSTRACT Cyanobacterial phycobilisomes (PBSs) are photosynthetic antenna complexes that harvest light energy and supply it to two reaction centers (RCs) where photochemistry starts. PBSs can be classified into two types, depending on the presence of allophycocyanin (APC): CpcG-PBS and CpcL-PBS. Because the accurate protein composition of CpcL-PBS remains unclear, we describe here its isolation and characterization from the cyanobacterium Synechocystis sp. strain 6803. We found that ferredoxin-NADP+ oxidoreductase (or FNRL), an enzyme involved in both cyclic electron transport and the terminal step of the electron transport chain in oxygenic photosynthesis, is tightly associated with CpcL-PBS as well as with CpcG-PBS. Room temperature and low-temperature fluorescence analyses show a red-shifted emission at 669 nm in CpcL-PBS as a terminal energy emitter without APC. SDS-PAGE and quantitative mass spectrometry reveal an increased content of FNRL and CpcC2, a rod linker protein, in CpcL-PBS compared to that of CpcG-PBS rods, indicative of an elongated CpcL-PBS rod length and its potential functional differences from CpcG-PBS. Furthermore, we combined isotope-encoded cross-linking mass spectrometry with computational protein structure predictions and structural modeling to produce an FNRL-PBS binding model that is supported by two cross-links between K69 of FNRL and the N terminus of CpcB, one component in PBS, in both CpcG-PBS and CpcL-PBS (cross-link 1), and between the N termini of FNRL and CpcB (cross-link 2). Our data provide a novel functional assembly form of phycobiliproteins and a molecular-level description of the close association of FNRL with phycocyanin in both CpcG-PBS and CpcL-PBS. IMPORTANCE Cyanobacterial light-harvesting complex PBSs are essential for photochemistry in light reactions and for balancing energy flow to carbon fixation in the form of ATP and NADPH. We isolated a new type of PBS without an allophycocyanin core (i.e., CpcL-PBS). CpcL-PBS contains both a spectral red-shifted chromophore, enabling efficient energy transfer to chlorophyll molecules in the reaction centers, and an increased FNRL content with various rod lengths. Identification of a close association of FNRL with both CpcG-PBS and CpcL-PBS brings new insight to its regulatory role for fine-tuning light energy transfer and carbon fixation through both noncyclic and cyclic electron transport.

Download Full-text

Identification of the quinone species in cyanide-sensitive and cyanide-insensitive mitochondria of Moniliella tomentosa

Biochemical Journal ◽

10.1042/bj1920881 ◽

1980 ◽

Vol 192 (3) ◽

pp. 881-885 ◽

Cited By ~ 13

Author(s):

J Vanderleyden ◽

M Meyers ◽

H Verachtert

Keyword(s):

Electron Transport ◽

Oxidase Activity ◽

Alternative Oxidase ◽

Transport Pathways ◽

Naturally Occurring

Moniliella tomentosa was investigated for the presence of different quinones that might be involved in the cyanide-sensitive and/or cyanide-insensitive electron-transport pathways. The naturally occurring quinone in Moniliella tomentosa was found to be ubiquinone-45. Other quinone species could not be detected. The concentration of ubiquinone-45 in mitochondria is not related to the presence or absence of the alternative oxidase activity.

Download Full-text

The relationship of the cyclic and non-cyclic electron transport pathways in chloroplasts

Biochimica et Biophysica Acta (BBA) - Bioenergetics ◽

10.1016/0005-2728(80)90169-3 ◽

1980 ◽

Vol 591 (2) ◽

pp. 381-390 ◽

Cited By ~ 21

Author(s):

Richard Malkin ◽

Richard K. Chain

Keyword(s):

Electron Transport ◽

Cyclic Electron Transport ◽

Transport Pathways ◽

Relationship Of ◽

The Relationship

Download Full-text

The Significance of Chloroplast NAD(P)H Dehydrogenase Complex and Its Dependent Cyclic Electron Transport in Photosynthesis

Frontiers in Plant Science ◽

10.3389/fpls.2021.661863 ◽

2021 ◽

Vol 12 ◽

Author(s):

Mingzhu Ma ◽

Yifei Liu ◽

Chunming Bai ◽

Jean Wan Hong Yong

Keyword(s):

Electron Transport ◽

Growth And Development ◽

Redox System ◽

Thylakoid Membranes ◽

Plant Evolution ◽

Cyclic Electron Transport ◽

Plant Growth And Development ◽

Transport Pathways ◽

Electron Transfer Chain ◽

Transfer Chain

Chloroplast NAD(P)H dehydrogenase (NDH) complex, a multiple-subunit complex in the thylakoid membranes mediating cyclic electron transport, is one of the most important alternative electron transport pathways. It was identified to be essential for plant growth and development during stress periods in recent years. The NDH-mediated cyclic electron transport can restore the over-reduction in stroma, maintaining the balance of the redox system in the electron transfer chain and providing the extra ATP needed for the other biochemical reactions. In this review, we discuss the research history and the subunit composition of NDH. Specifically, the formation and significance of NDH-mediated cyclic electron transport are discussed from the perspective of plant evolution and physiological functionality of NDH facilitating plants’ adaptation to environmental stress. A better understanding of the NDH-mediated cyclic electron transport during photosynthesis may offer new approaches to improving crop yield.

Download Full-text

Structures of nitroaromatic compounds induce Shewanella oneidensis MR-1 to adopt different electron transport pathways to reduce the contaminants

Journal of Hazardous Materials ◽

10.1016/j.jhazmat.2019.121495 ◽

2020 ◽

Vol 384 ◽

pp. 121495 ◽

Cited By ~ 2

Author(s):

Hefei Wang ◽

He-Ping Zhao ◽

Lizhong Zhu

Keyword(s):

Electron Transport ◽

Shewanella Oneidensis ◽

Nitroaromatic Compounds ◽

Transport Pathways

Download Full-text

Inhibition of xanthine oxidase ameliorates functional and metabolic impairment in type 2 diabetic hearts under pressure overload

European Heart Journal ◽

10.1093/ehjci/ehaa946.3618 ◽

2020 ◽

Vol 41 (Supplement_2) ◽

Author(s):

Y Igaki ◽

A Osanami ◽

M Tanno ◽

T Sato ◽

T Ogawa ◽

...

Keyword(s):

Diastolic Dysfunction ◽

Xanthine Oxidase ◽

Adenine Nucleotide ◽

Vascular Dysfunction ◽

Pressure Overload ◽

Diabetic Control ◽

Funding Source ◽

National Budget ◽

Adenine Nucleotide Pool

Abstract Background We recently reported that upregulated AMP deaminase (AMPD), via reduction in the tissue adenine nucleotide pool, contributes to exacerbation of diastolic dysfunction under pressure overload in OLETF, a rat model of obese type 2 diabetes (T2DM). Upregulated AMPD also possibly promotes xanthine oxidase (XO)-mediated ROS production, since AMPD deaminases AMP to IMP, which is further converted to inosine, providing substrates of XO, hypoxanthine and xanthine. Here, we examined the hypothesis that inhibition of XO ameliorates the pressure overload-induced diastolic dysfunction by suppression of ROS-mediated mitochondrial dysfunction and/or vascular dysfunction in T2DM rats. Methods and results Metabolomic analyses revealed that levels of xanthine and uric acid in the LV myocardium were significantly higher by 37% and 51%, respectively, in OLETF than in LETO, non-diabetic control rats, under the condition of phenylephrine-induced pressure overloading (200–230 mmHg). Myocardial XO activity in OLETF was 57.9% higher than that in LETO, which may be attributed to 31% higher level of inosine, a positive regulator of XO, in OLETF than in LETO. The activity of XO was significantly attenuated by administration of topiroxostat, an XO inhibitor at 0.5 mg/kg/day for 14 days. Pressure volume loop analyses showed that the pressure overloading resulted in significantly higher LVEDP in OLETF than in LETO (18.3±1.5 vs. 12.2±1.3 mmHg, p<0.05, n=7), though LVEDPs at baseline were comparable in OLETF and LETO (5.6±0.4 vs. 4.7±0.7 mmHg). Treatment with topiroxostat significantly suppressed the pressure overload-induced elevation of LVEDP in OLETF (18.3±1.5 vs. 11.3±1.1 mmHg, p<0.05) but not in LETO. Under the condition of pressure overloading, Ea/Ees, an index for ventricular-arterial coupling, was higher in OLETF than in LETO (2.3±0.3 vs. 1.6±0.3, p<0.05), and it was also improved by topiroxostat in OLETF (1.2±0.2, p<0.05). Myocardial ATP content was lower in OLETF than in LETO (2966±400 vs. 1818±171 nmol/g wet tissue, p<0.05), and treatment with topiroxostat significantly restored the ATP level (2629±307 nmol/g wet tissue). The LV myocardium of OLETF under pressure overload showed significantly higher level of malondialdehyde and 4-hydroxynonenal, an indicator of lipid peroxidation, than that of LETO. Measurement of oxygen consumption rate by Seahorse XFe96 Analyzer in mitochondria isolated from LV tissues revealed that state 3 respiration was significantly suppressed in OLETF by 43% compared to LETO, and it was restored by treatment with topiroxostat. Conclusion Both activity and substrates of XO are increased in T2DM hearts, in which upregulation of AMPD may play a role. Inhibition of XO ameliorates pressure overload-induced diastolic dysfunction and improves ventricular-arterial coupling in diabetic hearts, most likely through protection of mitochondrial function from ROS-mediated injury. Funding Acknowledgement Type of funding source: Public grant(s) – National budget only. Main funding source(s): Grant-in-aid for Scientific Research (#26461132, #17K09584) from the Japanese Society for the Promotion of Science

Download Full-text

Electron transport pathways for the oxidation of endogenous substrate(s) in Acidithiobacillus ferrooxidans

Canadian Journal of Microbiology ◽

10.1139/w05-128 ◽

2006 ◽

Vol 52 (4) ◽

pp. 317-327 ◽

Cited By ~ 4

Author(s):

Yongqiang Chen ◽

Isamu Suzuki

Keyword(s):

Electron Transport ◽

Electron Acceptor ◽

Acidithiobacillus Ferrooxidans ◽

Complex I ◽

Iron Chelators ◽

Endogenous Respiration ◽

Sugar Alcohols ◽

Transport Pathways ◽

Endogenous Substrate ◽

Transport Inhibitors

Oxidation of endogenous substrate(s) of Acidithiobacillus ferrooxidans with O2 or Fe3+ as electron acceptor was studied in the presence of uncouplers and electron transport inhibitors. Endogenous substrate was oxidized with a respiratory quotient (CO2 produced/O2 consumed) of 1.0, indicating its carbohydrate nature. The oxidation was inhibited by complex I inhibitors (rotenone, amytal, and piericidin A) only partially, but piericidin A inhibited the oxidation with Fe3+ nearly completely. The oxidation was stimulated by uncouplers, and the stimulated activity was more sensitive to inhibition by complex I inhibitors. HQNO (2-heptyl-4-hydroxyquinoline N-oxide) also stimulated the oxidation, and the stimulated respiration was more sensitive to KCN inhibition than uncoupler stimulated respiration. Fructose, among 20 sugars and sugar alcohols including glucose and mannose, was oxidized with a CO2/O2 ratio of 1.0 by the organism. Iron chelators in general stimulated endogenous respiration, but some of them reduced Fe3+ chemically, introducing complications. The results are discussed in view of a branched electron transport system of the organism and its possible control.Key words: Acidithiobacillus ferrooxidans, endogenous respiration, uncouplers, electron transport.

Download Full-text

The role of glutamine oxidation and the purine nucleotide cycle for adaptation of tumour energetics to the transition from the anaerobic to the aerobic state

Biochemical Journal ◽

10.1042/bj2520381 ◽

1988 ◽

Vol 252 (2) ◽

pp. 381-386 ◽

Cited By ~ 7

Author(s):

Z Kovacević ◽

D Jerance ◽

O Brkljac

Keyword(s):

Adenine Nucleotide ◽

The Other ◽

Purine Nucleotide ◽

Purine Nucleotide Cycle ◽

Adenine Nucleotide Pool

It is proposed that the purine nucleotide cycle and glutamine oxidation play a key role in the adaptation of tumour energetics to the transition from the anaerobic to the aerobic state. In support of this proposal, it was found that glutamine and inosine markedly increase total adenylates in the presence of oxygen, whereas the addition of hadacidin abolishes this effect. Transition of the cells from the anaerobic to the aerobic state, and vice versa, in the presence of glutamine plus inosine revealed that there are two components of the adenine nucleotide pool, one which is stable and the other which is variable and responds to the aerobic-anaerobic transition. This part of the pool undergoes degradation or resynthesis owing to activation of the enzymes of the purine nucleotide cycle. Resynthesis of the pool is accompanied by substantial net utilization of aspartate, which is produced by glutamine oxidation. This is supported by the experiments in which the cells were alternately incubated with nitrogen or oxygen, demonstrating that hadacidin significantly decreased utilization of aspartate and regeneration of ATP owing to inhibition of adenylosuccinate synthase.

Download Full-text