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      Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes ☆

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          Abstract

          The cyanobacterial thylakoid membrane represents a system that can carry out both oxygenic photosynthesis and respiration simultaneously. The organization, interactions and mobility of components of these two electron transport pathways are indispensable to the biosynthesis of thylakoid membrane modules and the optimization of bioenergetic electron flow in response to environmental changes. These are of fundamental importance to the metabolic robustness and plasticity of cyanobacteria. This review summarizes our current knowledge about the distribution and dynamics of electron transport components in cyanobacterial thylakoid membranes. Global understanding of the principles that govern the dynamic regulation of electron transport pathways in nature will provide a framework for the design and synthetic engineering of new bioenergetic machinery to improve photosynthesis and biofuel production. This article is part of a Special Issue entitled: Organization and dynamics of bioenergetic systems in bacteria, edited by Conrad Mullineaux.

          Highlights

          • •

            Cyanobacterial thylakoid membranes carry out both oxygenic photosynthesis and respiration.

          • •

            Electron transport components are located in the thylakoid membrane and functionally coordinate with each other.

          • •

            Distribution and dynamics of electron transport components are physiologically regulated in response to environmental change.

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          Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis.

          Masakazu Iwai, Kenji Takizawa, Ryutaro Tokutsu … (2010)
          Photosynthetic light reactions establish electron flow in the chloroplast's thylakoid membranes, leading to the production of the ATP and NADPH that participate in carbon fixation. Two modes of electron flow exist-linear electron flow (LEF) from water to NADP(+) via photosystem (PS) II and PSI in series and cyclic electron flow (CEF) around PSI (ref. 2). Although CEF is essential for satisfying the varying demand for ATP, the exact molecule(s) and operational site are as yet unclear. In the green alga Chlamydomonas reinhardtii, the electron flow shifts from LEF to CEF on preferential excitation of PSII (ref. 3), which is brought about by an energy balancing mechanism between PSII and PSI (state transitions). Here, we isolated a protein supercomplex composed of PSI with its own light-harvesting complex (LHCI), the PSII light-harvesting complex (LHCII), the cytochrome b(6)f complex (Cyt bf), ferredoxin (Fd)-NADPH oxidoreductase (FNR), and the integral membrane protein PGRL1 (ref. 5) from C. reinhardtii cells under PSII-favouring conditions. Spectroscopic analyses indicated that on illumination, reducing equivalents from downstream of PSI were transferred to Cyt bf, whereas oxidised PSI was re-reduced by reducing equivalents from Cyt bf, indicating that this supercomplex is engaged in CEF (Supplementary Fig. 1). Thus, formation and dissociation of the PSI-LHCI-LHCII-FNR-Cyt bf-PGRL1 supercomplex not only controlled the energy balance of the two photosystems, but also switched the mode of photosynthetic electron flow.
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            A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria.

            Ghada Ajlani, Imre Vass, Jean-Marc Verbavatz … (2006)
            Photosynthetic organisms have developed multiple protective mechanisms to survive under high-light conditions. In plants, one of these mechanisms is the thermal dissipation of excitation energy in the membrane-bound chlorophyll antenna of photosystem II. The question of whether or not cyanobacteria, the progenitor of the chloroplast, have an equivalent photoprotective mechanism has long been unanswered. Recently, however, evidence was presented for the possible existence of a mechanism dissipating excess absorbed energy in the phycobilisome, the extramembrane antenna of cyanobacteria. Here, we demonstrate that this photoprotective mechanism, characterized by blue light-induced fluorescence quenching, is indeed phycobilisome-related and that a soluble carotenoid binding protein, ORANGE CAROTENOID PROTEIN (OCP), encoded by the slr1963 gene in Synechocystis PCC 6803, plays an essential role in this process. Blue light is unable to quench fluorescence in the absence of phycobilisomes or OCP. The fluorescence quenching is not DeltapH-dependent, and it can be induced in the absence of the reaction center II or the chlorophyll antenna, CP43 and CP47. Our data suggest that OCP, which strongly interacts with the thylakoids, acts as both the photoreceptor and the mediator of the reduction of the amount of energy transferred from the phycobilisomes to the photosystems. These are novel roles for a soluble carotenoid protein.
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              Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria.

              Haijun Liu, Hao Zhang, Dariusz M. Niedzwiedzki … (2013)
              In photosynthetic organisms, photons are captured by light-harvesting antenna complexes, and energy is transferred to reaction centers where photochemical reactions take place. We describe here the isolation and characterization of a fully functional megacomplex composed of a phycobilisome antenna complex and photosystems I and II from the cyanobacterium Synechocystis PCC 6803. A combination of in vivo protein cross-linking, mass spectrometry, and time-resolved spectroscopy indicates that the megacomplex is organized to facilitate energy transfer but not intercomplex electron transfer, which requires diffusible intermediates and the cytochrome b6f complex. The organization provides a basis for understanding how phycobilisomes transfer excitation energy to reaction centers and how the energy balance of two photosystems is achieved, allowing the organism to adapt to varying ecophysiological conditions.
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                Author and article information

                Contributors
                Lu-Ning Liu
                Journal
                Journal ID (nlm-ta): Biochim Biophys Acta
                Journal ID (iso-abbrev): Biochim. Biophys. Acta
                Title: Biochimica et Biophysica Acta
                Publisher: Elsevier Pub. Co
                ISSN (Print): 0006-3002
                Publication date PMC-release: 1 March 2016
                Publication date (Print): March 2016
                Volume: 1857
                Issue: 3
                Pages: 256-265
                Affiliations
                Institute of Integrative Biology, University of Liverpool, Crown Street, Liverpool L69 7ZB, United Kingdom
                Article
                Publisher ID: S0005-2728(15)00242-X
                DOI: 10.1016/j.bbabio.2015.11.010
                PMC ID: 4756276
                PubMed ID: 26619924
                SO-VID: 1f8ca093-922e-45e1-a8e5-2fb408c0736f
                Copyright © © 2015 The Author
                License:

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 15 July 2015
                Date revision received : 17 November 2015
                Date accepted : 19 November 2015
                Categories
                Subject: Article

                ScienceOpen disciplines: Biochemistry
                Keywords: cyanobacteria,electron transport,membrane protein,photosynthesis,protein distribution,protein dynamics,respiration,supramolecular complex,thylakoid membrane
                Data availability:
                ScienceOpen disciplines: Biochemistry
                Keywords: cyanobacteria, electron transport, membrane protein, photosynthesis, protein distribution, protein dynamics, respiration, supramolecular complex, thylakoid membrane

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