Cytochrome b6f complex

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Cytochrome b6f complex
1q90 opm.png
Crystal structure of the cytochrome b6f complex from C. reinhardtii ( 1q90 ). Hydrocarbon boundaries of the lipid bilayer are shown by red and blue lines (thylakoid space side and stroma side, respectively).
Identifiers
SymbolB6F
Pfam PF05115
InterPro IPR007802
TCDB 3.D.3
OPM superfamily 92
OPM protein 4pv1
Membranome 258
Available protein structures:
Pfam   structures / ECOD  
PDB RCSB PDB; PDBe; PDBj
PDBsum structure summary
Cytochrome b6f complex
Identifiers
EC no. 7.1.1.6
CAS no. 79079-13-3
Alt. namesPlastoquinol/plastocyanin reductase
Databases
IntEnz IntEnz view
BRENDA BRENDA entry
ExPASy NiceZyme view
KEGG KEGG entry
MetaCyc metabolic pathway
PRIAM profile
PDB structures RCSB PDB PDBe PDBsum
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PMC articles
PubMed articles
NCBI proteins

The cytochrome b6f complex (plastoquinol/plastocyanin reductase or plastoquinol/plastocyanin oxidoreductase; EC 7.1.1.6) is an enzyme found in the thylakoid membrane in chloroplasts of plants, cyanobacteria, and green algae, that catalyzes the transfer of electrons from plastoquinol to plastocyanin:

Contents

plastoquinol + 2 oxidized plastocyanin + 2 H+ [side 1] plastoquinone + 2 reduced plastocyanin + 4 H+ [side 2]. [1]

The reaction is analogous to the reaction catalyzed by cytochrome bc1 (Complex III) of the mitochondrial electron transport chain. During photosynthesis, the cytochrome b6f complex is one step along the chain that transfers electrons from Photosystem II to Photosystem I, and at the same time pumps protons into the thylakoid space, contributing to the generation of an electrochemical (energy) gradient [2] that is later used to synthesize ATP from ADP.

Enzyme structure

The cytochrome b6f complex is a dimer, with each monomer composed of eight subunits. [3] These consist of four large subunits: a 32 kDa cytochrome f with a c-type cytochrome, a 25 kDa cytochrome b6 with a low- and high-potential heme group, a 19 kDa Rieske iron-sulfur protein containing a [2Fe-2S] cluster, and a 17 kDa subunit IV; along with four small subunits (3-4 kDa): PetG, PetL, PetM, and PetN. [3] [4] The total molecular weight is 217 kDa.

The crystal structures of cytochrome b6f complexes from Chlamydomonas reinhardtii, Mastigocladus laminosus, and Nostoc sp. PCC 7120 have been determined. [2] [5] [6] [7] [8] [9]

The core of the complex is structurally similar to the cytochrome bc1 core. Cytochrome b6 and subunit IV are homologous to cytochrome b, [10] and the Rieske iron-sulfur proteins of the two complexes are homologous. [11] However, cytochrome f and cytochrome c1 are not homologous. [12]

Cytochrome b6f contains seven prosthetic groups. [13] [14] Four are found in both cytochrome b6f and bc1: the c-type heme of cytochrome c1 and f, the two b-type hemes (bp and bn) in bc1 and b6f, and the [2Fe-2S] cluster of the Rieske protein. Three unique prosthetic groups are found in cytochrome b6f: chlorophyll a, β-carotene, and heme cn (also known as heme x). [5]

The inter-monomer space within the core of the cytochrome b6f complex dimer is occupied by lipids, [9] which provides directionality to heme-heme electron transfer through modulation of the intra-protein dielectric environment. [15]

Biological function

Tobacco (Nicotiana tabacum) cytochrome b6f mutant (right) next to normal plant. Plants are used in photosynthesis research to investigate the cyclic photophosphorylation. Tobacco (Nicotiana tabacum) cyt6bf mutant.jpg
Tobacco ( Nicotiana tabacum ) cytochrome b6f mutant (right) next to normal plant. Plants are used in photosynthesis research to investigate the cyclic photophosphorylation.

In photosynthesis, the cytochrome b6f complex functions to mediate the transfer of electrons and of energy between the two photosynthetic reaction center complexes, Photosystem II and Photosystem I, while transferring protons from the chloroplast stroma across the thylakoid membrane into the lumen. [2] Electron transport via cytochrome b6f is responsible for creating the proton gradient that drives the synthesis of ATP in chloroplasts. [4]

In a separate reaction, the cytochrome b6f complex plays a central role in cyclic photophosphorylation, when NADP+ is not available to accept electrons from reduced ferredoxin. [16] This cycle, driven by the energy of P700 +, contributes to the creation of a proton gradient that can be used to drive ATP synthesis. It has been shown that this cycle is essential for photosynthesis, [17] helping to maintain the proper ratio of ATP/NADPH production for carbon fixation. [18] [19]

The p-side quinol deprotonation-oxidation reactions within the cytochrome b6f complex have been implicated in the generation of reactive oxygen species. [20] An integral chlorophyll molecule located within the quinol oxidation site has been suggested to perform a structural, non-photochemical function in enhancing the rate of formation of the reactive oxygen species, possibly to provide a redox-pathway for intra-cellular communication. [21]

Reaction mechanism

The cytochrome b6f complex is responsible for "non-cyclic" (1) and "cyclic" (2) electron transfer between two mobile redox carriers, plastoquinol (QH2) and plastocyanin (Pc):

H2O→photosystem II→QH2→Cyt b6f→Pc→photosystem I→NADPH(1)
QH2→Cyt b6f→Pc→photosystem I→Q(2)

Cytochrome b6f catalyzes the transfer of electrons from plastoquinol to plastocyanin, while pumping two protons from the stroma into the thylakoid lumen:

QH2 + 2Pc(Cu2+) + 2H+ (stroma) → Q + 2Pc(Cu+) + 4H+ (lumen) [16]

This reaction occurs through the Q cycle as in Complex III. [22] Plastoquinol acts as the electron carrier, transferring its two electrons to high- and low-potential electron transport chains (ETC) via a mechanism called electron bifurcation. [23] The complex contains up to three plastoquinone molecules that form an electron transfer network that are responsible for the operation of the Q cycle and its redox-sensing and catalytic functions in photosynthesis. [24]

Q cycle

Q cycle of cytochrome b6f Q-cycle cytochrome b6f.png
Q cycle of cytochrome b6f

First half of Q cycle

  1. QH2 binds to the positive 'p' side (lumen side) of the complex. It is oxidized to a semiquinone (SQ) by the iron-sulfur center (high-potential ETC) and releases two protons to the thylakoid lumen[ citation needed ].
  2. The reduced iron-sulfur center transfers its electron through cytochrome f to Pc.
  3. In the low-potential ETC, SQ transfers its electron to heme bp of cytochrome b6.
  4. Heme bp then transfers the electron to heme bn.
  5. Heme bn reduces Q with one electron to form SQ.

Second half of Q cycle

  1. A second QH2 binds to the complex.
  2. In the high-potential ETC, one electron reduces another oxidized Pc.
  3. In the low-potential ETC, the electron from heme bn is transferred to SQ, and the completely reduced Q2− takes up two protons from the stroma to form QH2.
  4. The oxidized Q and the reduced QH2 that has been regenerated diffuse into the membrane.

Cyclic electron transfer

Unlike Complex III, cytochrome b6f catalyzes another electron transfer reaction that is central to cyclic photophosphorylation. The electron from ferredoxin (Fd) is transferred to plastoquinone and then the cytochrome b6f complex to reduce plastocyanin, which is reoxidized by P700 in Photosystem I. [25] The exact mechanism of the reduction of plastoquinone by ferredoxin is still under investigation. One proposal is that there exists a ferredoxin:plastoquinone-reductase or an NADP dehydrogenase. [25] Since heme x does not appear to be required for the Q cycle and is not found in Complex III, it has been proposed that it is used for cyclic photophosphorylation by the following mechanism: [23] [26]

  1. Fd (red) + heme x (ox) → Fd (ox) + heme x (red)
  2. heme x (red) + Fd (red) + Q + 2H+ → heme x (ox) + Fd (ox) + QH2

Related Research Articles

<span class="mw-page-title-main">Cytochrome</span> Redox-active proteins containing a heme with a Fe atom as a cofactor

Cytochromes are redox-active proteins containing a heme, with a central iron (Fe) atom at its core, as a cofactor. They are involved in the electron transport chain and redox catalysis. They are classified according to the type of heme and its mode of binding. Four varieties are recognized by the International Union of Biochemistry and Molecular Biology (IUBMB), cytochromes a, cytochromes b, cytochromes c and cytochrome d.

<span class="mw-page-title-main">Photosynthesis</span> Biological process to convert light into chemical energy

Photosynthesis is a biological process used by many cellular organisms to convert light energy into chemical energy, which is stored in organic compounds that can later be metabolized through cellular respiration to fuel the organism's activities. The term usually refers to oxygenic photosynthesis, where oxygen is produced as a byproduct and some of the chemical energy produced is stored in carbohydrate molecules such as sugars, starch, glycogen and cellulose, which are synthesized from endergonic reaction of carbon dioxide with water. Most plants, algae and cyanobacteria perform photosynthesis; such organisms are called photoautotrophs. Photosynthesis is largely responsible for producing and maintaining the oxygen content of the Earth's atmosphere, and supplies most of the biological energy necessary for complex life on Earth.

A proton pump is an integral membrane protein pump that builds up a proton gradient across a biological membrane. Proton pumps catalyze the following reaction:

<span class="mw-page-title-main">Thylakoid</span> Membrane enclosed compartments in chloroplasts and cyanobacteria

Thylakoids are membrane-bound compartments inside chloroplasts and cyanobacteria. They are the site of the light-dependent reactions of photosynthesis. Thylakoids consist of a thylakoid membrane surrounding a thylakoid lumen. Chloroplast thylakoids frequently form stacks of disks referred to as grana. Grana are connected by intergranal or stromal thylakoids, which join granum stacks together as a single functional compartment.

<span class="mw-page-title-main">Plastoquinone</span> Molecule which moves electron in photosynthesis

Plastoquinone (PQ) is an isoprenoid quinone molecule involved in the electron transport chain in the light-dependent reactions of photosynthesis. The most common form of plastoquinone, known as PQ-A or PQ-9, is a 2,3-dimethyl-1,4-benzoquinone molecule with a side chain of nine isoprenyl units. There are other forms of plastoquinone, such as ones with shorter side chains like PQ-3 as well as analogs such as PQ-B, PQ-C, and PQ-D, which differ in their side chains. The benzoquinone and isoprenyl units are both nonpolar, anchoring the molecule within the inner section of a lipid bilayer, where the hydrophobic tails are usually found.

<span class="mw-page-title-main">Photosystem</span> Structural units of protein involved in photosynthesis

Photosystems are functional and structural units of protein complexes involved in photosynthesis. Together they carry out the primary photochemistry of photosynthesis: the absorption of light and the transfer of energy and electrons. Photosystems are found in the thylakoid membranes of plants, algae, and cyanobacteria. These membranes are located inside the chloroplasts of plants and algae, and in the cytoplasmic membrane of photosynthetic bacteria. There are two kinds of photosystems: PSI and PSII.

<span class="mw-page-title-main">Photosystem II</span> First protein complex in light-dependent reactions of oxygenic photosynthesis

Photosystem II is the first protein complex in the light-dependent reactions of oxygenic photosynthesis. It is located in the thylakoid membrane of plants, algae, and cyanobacteria. Within the photosystem, enzymes capture photons of light to energize electrons that are then transferred through a variety of coenzymes and cofactors to reduce plastoquinone to plastoquinol. The energized electrons are replaced by oxidizing water to form hydrogen ions and molecular oxygen.

<span class="mw-page-title-main">Photosystem I</span> Second protein complex in photosynthetic light reactions

Photosystem I is one of two photosystems in the photosynthetic light reactions of algae, plants, and cyanobacteria. Photosystem I is an integral membrane protein complex that uses light energy to catalyze the transfer of electrons across the thylakoid membrane from plastocyanin to ferredoxin. Ultimately, the electrons that are transferred by Photosystem I are used to produce the moderate-energy hydrogen carrier NADPH. The photon energy absorbed by Photosystem I also produces a proton-motive force that is used to generate ATP. PSI is composed of more than 110 cofactors, significantly more than Photosystem II.

<span class="mw-page-title-main">Photophosphorylation</span> Biochemical process in photosynthesis

In the process of photosynthesis, the phosphorylation of ADP to form ATP using the energy of sunlight is called photophosphorylation. Cyclic photophosphorylation occurs in both aerobic and anaerobic conditions, driven by the main primary source of energy available to living organisms, which is sunlight. All organisms produce a phosphate compound, ATP, which is the universal energy currency of life. In photophosphorylation, light energy is used to pump protons across a biological membrane, mediated by flow of electrons through an electron transport chain. This stores energy in a proton gradient. As the protons flow back through an enzyme called ATP synthase, ATP is generated from ADP and inorganic phosphate. ATP is essential in the Calvin cycle to assist in the synthesis of carbohydrates from carbon dioxide and NADPH.

<span class="mw-page-title-main">Cytochrome f</span>

Cytochrome f is the largest subunit of cytochrome b6f complex. In its structure and functions, the cytochrome b6f complex bears extensive analogy to the cytochrome bc1 complex of mitochondria and photosynthetic purple bacteria. Cytochrome f plays a role analogous to that of cytochrome c1, in spite of their different structures.

<span class="mw-page-title-main">Rieske protein</span> Protein family with an iron–sulfur center transferring electrons

Rieske proteins are iron–sulfur protein (ISP) components of cytochrome bc1 complexes and cytochrome b6f complexes and are responsible for electron transfer in some biological systems. John S. Rieske and co-workers first discovered the protein and in 1964 isolated an acetylated form of the bovine mitochondrial protein. In 1979 Trumpower's lab isolated the "oxidation factor" from bovine mitochondria and showed it was a reconstitutively-active form of the Rieske iron-sulfur protein
It is a unique [2Fe-2S] cluster in that one of the two Fe atoms is coordinated by two histidine residues rather than two cysteine residues. They have since been found in plants, animals, and bacteria with widely ranging electron reduction potentials from -150 to +400 mV.

<span class="mw-page-title-main">Electrochemical gradient</span> Gradient of electrochemical potential, usually for an ion that can move across a membrane

An electrochemical gradient is a gradient of electrochemical potential, usually for an ion that can move across a membrane. The gradient consists of two parts:

<span class="mw-page-title-main">Q cycle</span>

The Q cycle describes a series of reactions that describe how the sequential oxidation and reduction of the lipophilic electron carrier Coenzyme Q (CoQ) between the ubiquinol and ubiquinone forms, can result in the net movement of protons across a lipid bilayer.

<span class="mw-page-title-main">Photosynthetic reaction centre</span> Molecular unit responsible for absorbing light in photosynthesis

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<span class="mw-page-title-main">Cytochrome b</span> Mitochondrial protein involved in the respiratory chain

Cytochrome b within both molecular and cell biology, is a protein found in the mitochondria of eukaryotic cells. It functions as part of the electron transport chain and is the main subunit of transmembrane cytochrome bc1 and b6f complexes.

Oxygenevolution is the process of generating molecular oxygen (O2) by a chemical reaction, usually from water. Oxygen evolution from water is effected by oxygenic photosynthesis, electrolysis of water, and thermal decomposition of various oxides. The biological process supports aerobic life. When relatively pure oxygen is required industrially, it is isolated by distilling liquefied air.

Dioxygen plays an important role in the energy metabolism of living organisms. Free oxygen is produced in the biosphere through photolysis of water during photosynthesis in cyanobacteria, green algae, and plants. During oxidative phosphorylation in cellular respiration, oxygen is reduced to water, thus closing the biological water-oxygen redox cycle.

<span class="mw-page-title-main">Light-dependent reactions</span> Photosynthetic reactions

Light-dependent reactions refers to certain photochemical reactions that are involved in photosynthesis, the main process by which plants acquire energy. There are two light dependent reactions, the first occurs at photosystem II (PSII) and the second occurs at photosystem I (PSI).

Plastid terminal oxidase or plastoquinol terminal oxidase (PTOX) is an enzyme that resides on the thylakoid membranes of plant and algae chloroplasts and on the membranes of cyanobacteria. The enzyme was hypothesized to exist as a photosynthetic oxidase in 1982 and was verified by sequence similarity to the mitochondrial alternative oxidase (AOX). The two oxidases evolved from a common ancestral protein in prokaryotes, and they are so functionally and structurally similar that a thylakoid-localized AOX can restore the function of a PTOX knockout.

Matthew Johnson is a Reader in Biochemistry at the University of Sheffield, England. He was the 2018 recipient of the Biochemical Society’s Colworth Medal.

References

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  3. 1 2 Whitelegge JP, Zhang H, Aguilera R, Taylor RM, Cramer WA (Oct 2002). "Full subunit coverage liquid chromatography electrospray ionization mass spectrometry (LCMS+) of an oligomeric membrane protein: cytochrome b(6)f complex from spinach and the cyanobacterium Mastigocladus laminosus". Molecular & Cellular Proteomics. 1 (10): 816–27. doi: 10.1074/mcp.m200045-mcp200 . PMID   12438564.
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  7. ↑ Baniulis D, Yamashita E, Whitelegge JP, Zatsman AI, Hendrich MP, Hasan SS, Ryan CM, Cramer WA (Apr 2009). "Structure-Function, Stability, and Chemical Modification of the Cyanobacterial Cytochrome b6f Complex from Nostoc sp. PCC 7120". The Journal of Biological Chemistry. 284 (15): 9861–9. doi: 10.1074/jbc.M809196200 . PMC   2665108 . PMID   19189962.
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  12. ↑ Martinez SE, Huang D, Szczepaniak A, Cramer WA, Smith JL (Feb 1994). "Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation". Structure. 2 (2): 95–105. doi: 10.1016/s0969-2126(00)00012-5 . PMID   8081747.
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  14. ↑ Cramer WA, Zhang H, Yan J, Kurisu G, Smith JL (May 2004). "Evolution of photosynthesis: time-independent structure of the cytochrome b6f complex". Biochemistry. 43 (20): 5921–9. doi:10.1021/bi049444o. PMID   15147175.
  15. ↑ Hasan SS, Zakharov SD, Chauvet A, Stadnytskyi V, Savikhin S, Cramer WA (Jun 2014). "A map of dielectric heterogeneity in a membrane protein: the hetero-oligomeric cytochrome b6f complex". The Journal of Physical Chemistry B. 118 (24): 6614–25. doi:10.1021/jp501165k. PMC   4067154 . PMID   24867491.
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  17. ↑ Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (Jun 2004). "Cyclic electron flow around photosystem I is essential for photosynthesis". Nature. 429 (6991): 579–82. doi:10.1038/nature02598. PMID   15175756. S2CID   4421776.
  18. ↑ Blankenship RE (2002). Molecular mechanisms of photosynthesis. Oxford ; Malden, MA: Blackwell Science. ISBN   978-0-632-04321-7.
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