Organization and Flexibility of Cyanobacterial Thylakoid Membranes Examined by Neutron Scattering

Liberton, Michelle; Page, Lawrence; O’Dell, William B.; O’Neill, Hugh; Mamontov, Eugene; Urban, Volker S.; Pakrasi, Himadri B.

doi:10.1074/jbc.m112.416933

Cited by 93 publications

(110 citation statements)

References 22 publications

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“…In general, these results, in line with similar observations [29,39,[41][42][43], underline the remarkable flexibility of the thylakoid membrane ultrastructure, which should thus not be portrayed as simply providing a scaffold for the photosynthetic functions but also actively participating in the energy conversion steps and in different regulatory functions.…”

Section: Resultssupporting

confidence: 78%

Low-pH induced reversible reorganizations of chloroplast thylakoid membranes — As revealed by small-angle neutron scattering

Ünnep¹,

Zsíros²,

Hörcsik³

et al. 2017

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Energization of thylakoid membranes brings about the acidification of the lumenal aqueous phase, which activates important regulatory mechanisms. Earlier Jajoo and coworkers (2014 FEBS Lett. 588:970) have shown that low pH in isolated plant thylakoid membranes induces changes in the excitation energy distribution between the two photosystems. In order to elucidate the structural background of these changes, we used small-angle neutron scattering on thylakoid membranes exposed to low p 2 H (pD) and show that gradually lowering the p 2 H from 8.0 to 5.0 causes small but well discernible reversible diminishment of the periodic order and the lamellar repeat distance and an increased mosaicity -similar to the effects elicited by light-induced acidification of the lumen. Our data strongly suggest that thylakoids dynamically respond to the membrane energization and actively participate in different regulatory mechanisms. Keywords: chloroplast thylakoid membranes, lamellar repeat distance, low pH and p 2 H, smallangle neutron scattering (SANS) Highlights:1. Thylakoid membranes exposed to low p 2 H studied by small-angle neutron scattering 2. Acidification causes reversible shrinkage and diminished lamellar order 3. SANS changes induced by low pH resemble those due to light-induced lumenal acidification Abbreviations: p 2 H (pD), deuterium analogue of pH; NPQ, non-photochemical quenching; qE, the energy-dependent component of NPQ; ∆µ H + , transmembrane electrochemical potential gradient; PSI, photosystem I; PSII, photosystem II; LET, linear electron transport; CD, circular dichroism; SANS, small-angle neutron scattering; q, scattering vector; I, intensity; q*, center position of the Bragg peak; RD, repeat distance; φ, azimuthal angle; I(φ), angular dependency of the scattering intensity; FWHM, full width at half maximum 3

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Section: Resultssupporting

confidence: 78%

Low-pH induced reversible reorganizations of chloroplast thylakoid membranes — As revealed by small-angle neutron scattering

Ünnep¹,

Zsíros²,

Hörcsik³

et al. 2017

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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“…In cyanobacteria, PSI turnover in PSI-enriched membrane domains requires that reduced plastocyanin or cytochrome c 6 molecules, generated by distal cytb 6 f complexes in the mixed membrane zones, diffuse to their docking sites on the lumenal side of the PSI array. Given that cyanobacterial thylakoids are closely appressed, and enclose a lumen of 5 to 9 nm (van de Meene et al, 2006;Liberton et al, 2013b), plastocyanin migration from cytb 6 f complexes and reduction of the PSI in large arrays might be impeded, as in plants. The cytochrome c 6 to PSI ratio for T. elongatus, for example, has been determined as 1.7 (Nguyen et al, 2017), so ensuring that they are oxidized by one of the PSI complexes in an array could be important.…”

Section: Discussionmentioning

confidence: 99%

Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids

et al. 2017

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Photosystem I (PSI) is the dominant photosystem in cyanobacteria and it plays a pivotal role in cyanobacterial metabolism. Despite its biological importance, the native organization of PSI in cyanobacterial thylakoid membranes is poorly understood. Here, we use atomic force microscopy (AFM) to show that ordered, extensive macromolecular arrays of PSI complexes are present in thylakoids from Thermosynechococcus elongatus, Synechococcus sp PCC 7002, and Synechocystis sp PCC 6803. Hyperspectral confocal fluorescence microscopy and three-dimensional structured illumination microscopy of Synechocystis sp PCC 6803 cells visualize PSI domains within the context of the complete thylakoid system. Crystallographic and AFM data were used to build a structural model of a membrane landscape comprising 96 PSI trimers and 27,648 chlorophyll a molecules. Rather than facilitating intertrimer energy transfer, the close associations between PSI primarily maximize packing efficiency; short-range interactions with Complex I and cytochrome b 6 f are excluded from these regions of the membrane, so PSI turnover is sustained by long-distance diffusion of the electron donors at the membrane surface. Elsewhere, PSI-photosystem II contact zones provide sites for docking phycobilisomes and the formation of megacomplexes. PSI-enriched domains in cyanobacteria might foreshadow the partitioning of PSI into stromal lamellae in plants, similarly sustained by long-distance diffusion of electron carriers.

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“…Well-defined Bragg diffraction peaks were previously reported between 0.02 and 0.035 Å -1 in isolated granal chloroplasts, cyanobacteria, and diatoms (11,18). However, SANS experiments on the dark-adapted WT Chlamydomonas cells could not reveal any distinct Bragg diffraction peak, but only a shoulder at ∼0.035 Å -1 , indicating a poorly defined RD of ∼180 Å (Fig.…”

Section: Small-angle Neutron Scattering Measurements Indicate That Statementioning

confidence: 67%

“…Earlier experiments performed on cyanobacterial and diatom cells (11,12,18) have shown that light exposure induces darkreversible changes in the thylakoid-membrane ultrastructure, affecting both the Bragg peaks and the high-Q peak, without inducing ST. To verify the existence of this phenomenon in Chlamydomonas, we performed experiments on the stt7-9 mutant, which is unable to perform STs (20). In dark-adapted stt7-9 cells, a strong Bragg peak at 0.033 Å -1 (RD = 190 Å) was found (Fig.…”

Section: Small-angle Neutron Scattering Measurements Indicate That Statementioning

confidence: 99%

Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo

Nagy

Ünnep

Zsíros

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

135

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Plants respond to changes in light quality by regulating the absorption capacity of their photosystems. These short-term adaptations use redox-controlled, reversible phosphorylation of the lightharvesting complexes (LHCIIs) to regulate the relative absorption cross-section of the two photosystems (PSs), commonly referred to as state transitions. It is acknowledged that state transitions induce substantial reorganizations of the PSs. However, their consequences on the chloroplast structure are more controversial. Here, we investigate how state transitions affect the chloroplast structure and function using complementary approaches for the living cells of Chlamydomonas reinhardtii. Using small-angle neutron scattering, we found a strong periodicity of the thylakoids in state 1, with characteristic repeat distances of ∼200 Å, which was almost completely lost in state 2. As revealed by circular dichroism, changes in the thylakoid periodicity were paralleled by modifications in the long-range order arrangement of the photosynthetic complexes, which was reduced by ∼20% in state 2 compared with state 1, but was not abolished. Furthermore, absorption spectroscopy reveals that the enhancement of PSI antenna size during state 1 to state 2 transition (∼20%) is not commensurate to the decrease in PSII antenna size (∼70%), leading to the possibility that a large part of the phosphorylated LHCIIs do not bind to PSI, but instead form energetically quenched complexes, which were shown to be either associated with PSII supercomplexes or in a free form. Altogether these noninvasive in vivo approaches allow us to present a more likely scenario for state transitions that explains their molecular mechanism and physiological consequences.green algae | photosynthesis | thylakoid membrane T he efficient operation of the photosynthetic machinery of oxygenic photosynthetic organisms requires a balanced energy supply to the two photosystems (PSs) under changing environments. To avoid unbalanced excitations of the two PSs, a rapid acclimation mechanism, state transitions (STs), takes place, which allows redistributing the excitation energy between the two PSs. ST is seen in green algae and vascular plants and is modulated by the redox-controlled, reversible phosphorylation of LHCII, the light-harvesting chlorophyll a/b antenna complex. A serine-threonine protein kinase, STN7 in vascular plants (1) and Stt7 in green algae (2), is responsible for this phosphorylation. Stt7/STN7 activity depends on the redox state of the plastoquinone (PQ) pool, which is sensed by the cytochrome b 6 f complex (3).According to the current model of STs, preferential PSII excitation leads to PQ reduction, and thus to LHCII phosphorylation by the kinase. The PQ pool can also be reduced in dark anaerobic conditions in algal suspensions. In this state, called state 2 (S2), phosphorylated LHCII dissociates from PSII, thereby reducing its absorption cross-section, and associates to PSI, acting as an additional antenna for this complex. In the reverse process, prefere...

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Organization and Flexibility of Cyanobacterial Thylakoid Membranes Examined by Neutron Scattering

Cited by 93 publications

References 22 publications

Low-pH induced reversible reorganizations of chloroplast thylakoid membranes — As revealed by small-angle neutron scattering

Low-pH induced reversible reorganizations of chloroplast thylakoid membranes — As revealed by small-angle neutron scattering

Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids

Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo

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