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Albanese, Pascal (2017) Structure and structural dynamics of Photosystem II supercomplex in higher plants. [Ph.D. thesis]

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Abstract (italian or english)

Photosynthesis is indisputably the primary biological process to introduce chemical energy and biomass into ecosystems by oxidizing water and reducing carbon dioxide into organic compounds. Photosystem II (PSII) is a unique protein complex, present in thylakoid membranes of all oxygenic photosynthetic organisms, able to catalyze the water-splitting reaction using sunlight as driving force, thus being responsible for the generation of all the molecular oxygen accumulated in the atmosphere for over three billion years. Although its catalytic core has been extremely conserved throughout evolution, from cyanobacteria to higher plants, the necessity of different photosynthetic organisms to cope with ever-changing environmental light conditions led to the emergence of a great variability among its peripheral antenna systems, differentiating in extrinsic phycobilisomes in cyanobacteria and intrinsic light harvesting complexes (LHCII) in green algae and higher plants.
LHCII are integral membrane proteins that occur as heterotrimers of Lhcb1-2-3 subunits and monomeric Lhcb4-5-6 polypeptides and associate peripherally with the PSII core in variable numbers, thus forming large supramolecular assemblies called PSII‐LHCII supercomplexes. The minimal functional unit, found in all light conditions, consists of a dimeric PSII core (C2) with two strongly bound LHCII trimers (S2), made of Lhcb1 and Lhcb2, connected by two monomeric Lhcb4 and Lhcb5 subunits, and is called C2S2. In limiting light conditions, the C2S2 can further associate with one or two moderately bound LHCII trimers (M2) which consist of Lhcb1, Lhcb2 and Lhcb3 proteins connected by the monomeric Lhcb6, a peculiar subunit found only in higher plants, originating supercomplexes of type C2S2M1-2. A further supramolecular organization is due to the lateral association of PSII-LHCII supercomplexes within the thylakoid membrane plane, forming PSII-LHCII megacomplexes, or even higher ordered arrays.
The LHCII fulfill a dual role by either quenching the excess light energy, often occurring in natural environments, or optimizing its harvesting in ecosystems where there is competition and mutual shading. The rearrangement of the PSII’s modular antenna system through its dynamic interaction with the PSII core, therefore, appears to be a key process in light harvesting regulation. Moreover, plant’s PSII and LHCII are spatially and functionally segregated into piled discs of thylakoid membranes (grana), where they occupy 80% of the surface. Their structural arrangement into PSII-LHCII supercomplexes interacting dynamically with each other appears to be critical in determining the overall membrane architecture and ultimately the efficiency of photosynthesis.
Although the overall structure of the basic C2S2 supercomplex in plants has been recently resolved at nearly atomic resolution, there is still a lack of knowledge regarding its structural rearrangement in different light conditions as well as its specific interaction within the membrane plane and between adjacent membranes.
During this thesis’ work we have been able to isolate pure PSII-LHCII super- and megacomplexes from pea plants grown in moderate light by mild solubilization of stacked thylakoid membranes. In order to assess their overall functional architecture, the full biochemical characterization of isolated PSII-LHCII supercomplexes, comprehensive of accurate proteomic analyses, was coupled with structural studies. Their structural characterization, performed by transmission electron microscopy (TEM) in cryogenic conditions (cryo-EM) and subsequent single particle analysis, led to a novel 3D structure at about 14 Å resolution of the supercomplexes of type C2S2M. The obtained electron density map revealed that under normal light conditions most of the supercomplexes within the grana are of type C2S2M and occur as paired supercomplexes, whose interactions are mediated by physical connections across the stromal gap of adjacent membranes. The specific overlapping of LHCII trimers facing each other in paired supercomplexes, as already observed in other studies, suggests that this conformation might be representative of their native state within the membranes. The physical connections observed across the stromal gap might be attributable to the mutual interaction between the long N-terminal loops of the monomeric Lhcb4 subunits. These subunits occupy a pivotal position in the 3D map of the paired supercomplexes and are clearly bridged across the stromal gap by electron densities attributable to these loops. In addition, despite the its structural flexibility, the remarkable sequence conservation of this region, even in distant phylogenetic photosynthetic organisms, may suggest its major involvement in structural dynamics. The specific interaction observed in paired supercomplexes seems to be mediated by cations present within the chloroplast in relatively low concentrations as their depletion from buffers used for isolation leads to the dissociation of the paired supercomplexes into single ones. Moreover, this evidence was also strongly supported by the decrease in the PSII excitonic connectivity measured in-vivo.
The paired behavior has also been observed in higher oligomerization forms of isolated PSII-LHCII supercomplexes in which two paired supercomplexes laterally interact with each other in the membrane plane, thus forming paired megacomplexes. This novel structure has been obtained by EM and 2D reconstruction of negatively stained particles and, despite its low resolution, reveals how PSII-LHCII supercomplexes may laterally and stromally interact with each other in different ways. The observation of the potential overlapping of LHCII trimers in megacomplexes facing each other, as well as the occurrence of different geometries of interaction between supercomplexes within the membrane plane and between megacomplexes in adjacent membranes, provide intriguing insights on how PSII and LHCII might interact in a very stable manner within the thylakoid membrane and between different discs in the grana.
In order to study the PSII-LHCII supercomplex remodeling in the context of ever-changing light environmental conditions, PSII-LHCII supercomplexes have been isolated from pea plants grown at different light intensities: low (LL), moderate (CL) and high light (HL). The accurate profiling and quantitation of the LHCII subunits in the isolated supercomplexes and in the native thylakoids, achieved by using a mass-spectrometry based proteomic approach, was coupled with the evaluation in-vivo of their functional antenna size (ASII). At increasing light intensities, the structural remodeling of the modular PSII’s antenna system led to the reduction of the amount of LHCII M-trimers in the isolated complexes, attested by the decreased level of Lhcb3 and Lhcb6. This specific remodeling does not occur at the same rate in the entire thylakoid membrane. The whole LHCII pool is downregulated only in plants grown in HL, suggesting the occurrence of different acclimation strategies. The remarkable decrease of the ASII observed in HL acclimated plants, when compared to LL plants, can be attributed to the significant increase of the Lhcb4 specific isoform Lhcb4.3, occurring both in isolated supercomplexes and in thylakoid membranes. Unlike isoforms Lhcb4.1-2, the Lhcb4.3 isoform, whose transcription is enhanced upon HL exposure, interestingly has a truncated C-terminus that is located at the binding interface with Lhcb6 within the supercomplex structure. The incorporation of Lhcb4.3 in the PSII-LHCII supercomplex might play a major role in decreasing its functional antenna size by reducing its affinity to bind additional M-trimers, thus regulating its light harvesting efficiency even at moderate light intensities. Conversely, the exposure to HL induces the decrease of the PSII antenna cross-section in isolated supercomplexes and the partial depletion of the whole antenna system of PSII in the thylakoid membranes, thus constitutively preventing damages to the reaction center when light continuously exceeds its energy-processing capacity. These results aim at broadening the current knowledge on how the light harvesting antenna system associated with the PSII core is finely regulated upon plants’ long term acclimation to different light intensities.
The flexibility of the PSII’s modular antenna system, accompanied by its finely tuned structural interaction with the core complex, pivotal for the 3D organization of plant thylakoid membranes, certainly played a key role in determining its remarkable evolutionary outcome. Taken together, these results may provide new research directions while certainly broadening the knowledge on how PSII-LHCII assemblies and their supramolecular interaction contribute to maintain the complex architecture of thylakoid membranes and the overall efficiency of photosynthesis in ever changing environmental conditions.

Abstract (a different language)

La fotosintesi è indubbiamente il processo biologico principale che introduce energia chimica e biomassa negli ecosistemi ossidando l’acqua e riducendo l'anidride carbonica in composti organici. Il fotosistema II (PSII) è un complesso proteico presente nelle membrane tilacoidali di tutti gli organismi fotosintetici, l’unico in grado di catalizzare la reazione di lisi dell'acqua utilizzando la luce solare come forza motrice e di conseguenza responsabile della generazione di tutto l'ossigeno molecolare presente nell'atmosfera da più di tre miliardi di anni. Nonostante il centro catalitico del PSII sia rimasto fondamentalmente inalterato nel corso dell'evoluzione dai cianobatteri alle piante superiori, la necessità di far fronte alla continua variazione delle condizioni di luce ambientali ha portato all’evoluzione di sistemi di antenne periferiche altamente differenziate, distinte in ficobilisomi estrinseci nei cianobatteri e complessi di membrana intrinseci (LHCII) in alghe verdi e piante superiori.
Gli LHCII sono complessi proteici di membrana presenti come etero-trimeri composti dalle subunità Lhcb1-2-3 e subunità monomeriche Lhcb4-5-6 associate perifericamente con il centro catalitico del PSII in numero variabile, formando così associazioni supramolecolari chiamate supercomplessi PSII-LHCII. L'unità funzionale minima, presente in ogni condizione di luce, detta C2S2, è costituita da un PSII centro di reazione dimerico (C2) legato strettamente a due complessi antenna trimerici (S2), composti da Lhcb1 e Lhcb2, mediante due subunità monomeriche Lhcb4 e Lhcb5. In condizioni di luce limitante il C2S2 può ulteriormente associare uno o due complessi antenna trimerici legati moderatamente (M2), costituiti dalle subunità Lhcb1, Lhcb2 e Lhcb3, mediante una peculiare subunità monomerica che si trova solo nelle piante superiori, Lhcb6, generando supercomplessi di tipo C2S2M1-2. I supercomplessi PSII-LHCII possono ulteriormente interagire lateralmente all'interno del piano della membrana tilacoidale formando megacomplessi PSII-LHCII o più estesi arrangiamenti ordinati semicristallini.
I complessi antenna LHCII svolgono un duplice ruolo, la dissipazione efficiente dell'energia luminosa, spesso in eccesso negli ambienti naturali, e l’ottimizzazione della sua raccolta negli ambienti in cui vi è concorrenza tra organismi e ombreggiatura reciproca. Il riassetto del sistema di antenne modulari del PSII attraverso la sua interazione dinamica con il centro catalitico sembra quindi essere un processo chiave nella regolazione della raccolta della luce. Inoltre, i PSII e LHCII nelle piante sono spazialmente e funzionalmente segregati in dischi impilati di membrane tilacoidi (grana), dove occupano l'80% della superficie. La loro disposizione strutturale in supercomplessi PSII-LHCII che interagiscono dinamicamente tra loro sembra essere determinante per l'architettura complessiva della membrana tilacoidale e quindi per l'efficienza della fotosintesi.
Sebbene la struttura del supercomplesso base C2S2 delle piante sia stata recentemente risolta ad una risoluzione quasi atomica, c'è ancora una lacuna conoscitiva riguardo al ri-arrangiamento strutturale dei PSII-LHCII che avviene in diverse condizioni di luce e alla loro interazione reciproca nel piano della membrana e tra membrane adiacenti dei grana.
Durante il lavoro svolto in questa tesi, siamo stati in grado di purificare super- e megacomplessi PSII-LHCII isolati da piante di pisello coltivate in luce moderata mediante la completa solubilizzazione delle membrane tilacoidali. La caratterizzazione biochimica dei supercomplessi PSII-LHCII isolati, complementata da accurate analisi proteomiche, è stata accoppiata con studi strutturali al fine di comprendere la loro architettura funzionale. La caratterizzazione strutturale, eseguita mediante microscopia elettronica a trasmissione (TEM) in condizioni criogeniche (cryo-EM) e successiva analisi d’immagine sulle singole particelle, ha portato ad una nuova struttura tridimensionale (3D) a circa 14 Å di risoluzione del supercomplesso di tipo C2S2M. La mappa di densità elettronica ottenuta ha rivelato che, in condizioni di luce di crescita di intensità moderata, la maggior parte dei supercomplessi è di tipo C2S2M. Essi sono disposti in maniera accoppiata, interagendo mediante collegamenti fisici attraverso l’intervallo stromatico, verosimilmente di membrane adiacenti. La sovrapposizione specifica degli LHCII trimerici, uno di fronte all'altro in supercomplessi accoppiati, come già osservato in altri studi, suggerisce che questa conformazione potrebbe essere rappresentativa del loro stato nativo all'interno delle membrane. I collegamenti fisici osservati nell’intervallo stromatico potrebbero essere attribuibili all'interazione reciproca tra le lunghe porzioni N-terminali di subunità monomeriche Lhcb4 adiacenti. Queste subunità occupano una posizione chiave nella mappa 3D dei supercomplessi accoppiati e le densità elettroniche che attraversano l’intervallo stromatico connettendo i due supercomplessi sono chiaramente attribuibili alle loro porzioni flessibili N-terminali. La sequenza amminoacidica di questa regione, nonostante la sua flessibilità, è sorprendentemente conservata anche in organismi fotosintetici filogeneticamente distanti, il che suggerisce un suo coinvolgimento in dinamiche strutturali fisiologicamente rilevanti per l’apparato fotosintetico. L'interazione specifica osservata nei supercomplessi appaiati sembra essere mediata dai cationi presenti all'interno del cloroplasto in concentrazioni fisiologiche. La loro rimozione dai tamponi utilizzati per l'isolamento, infatti, ne provoca la dissociazione in singoli supercomplessi. Questa evidenza è inoltre sostenuta dalla stima della connettività funzionale misurata in-vivo tramite tecniche di induzione di fluorescenza. Nei supercomplessi appaiati infatti si è evidenziato un potenziale trasferimento di energia maggiore se confrontato con i supercomplessi singolarizzati mediante semplice diluizione dei cationi presenti.
L’ appaiamento sul lato stromatico mediato da cationi è stato osservato anche in forme isolate di PSII-LHCII con forme di oligomerizzazione superiore ai supercomplessi, in cui due supercomplessi accoppiati interagiscono lateralmente tra loro nel piano di membrana, formando così megacomplessi appaiati. Questa nuova struttura è stata ottenuta con TEM e ricostruzione bidimensionale a partire da particelle colorate negativamente. Nonostante la bassa risoluzione ottenuta, questa struttura rivela come i supercomplessi PSII-LHCII possono interagire reciprocamente in modi diversi, sia lateralmente che attraverso l’intervallo stromatico. L'osservazione della potenziale sovrapposizione degli LHCII trimerici in megacomplessi accoppiati, così come la presenza di diverse geometrie di interazione tra supercomplessi all'interno del piano di membrana e tra megacomplessi nelle membrane adiacenti, forniscono informazioni interessanti su come PSII e LHCII potrebbero interagire in modo stabile e specifico all'interno della membrana tilacoidale e tra i vari dischi dei grana.
Al fine di studiare il rimodellamento dei supercomplessi PSII-LHCII nel contesto di un continuo cambiamento delle condizioni ambientali di luce, sono stati isolati supercomplessi PSII-LHCII da piante di pisello cresciute a diverse intensità di luce: bassa (LL), moderata (CL) e alta (HL). La valutazione in-vivo delle dimensioni dell'antenna funzionale del PSII (ASII) è stata accoppiata con l’identificazione e la quantificazione, mediante analisi proteomiche, delle diverse subunità di LHCII presenti sia nei supercomplessi isolati che nei tilacoidi nativi. All’aumentare dell’intensità di luce di crescita, si evince il rimodellamento strutturale dell’antenna modulare del PSII dovuto alla riduzione della quantità di LHCII trimerici di tipo “M” nei complessi isolati, attestata da una ridotta presenza di Lhcb3 e Lhcb6. Questo rimodellamento specifico non avviene però con le stesse modalità in tutta la membrana tilacoidale. Infatti, la quantità totale di LHCII nei tilacoidi viene significativamente ridotta solo in piante cresciute in HL, suggerendo la presenza di diverse strategie di acclimatazione in grado di ridurre l’antenna funzionale nei tilacoidi. La notevole diminuzione dell’ASII osservata sia nei supercomplessi isolati che nelle membrane tilacoidi di piante cresciute in HL, rispetto alle piante LL, può essere attribuita al significativo incremento di Lhcb4.3, una isoforma di Lhcb4. A differenza delle isoforme Lhcb4.1-2, l'isoforma Lhcb4.3, la cui trascrizione è nota aumentare in seguito all'esposizione ad HL, presenta l’estremità C-terminale troncata. Questa porzione della proteina nella struttura del supercomplesso C2S2M si trova a livello dell’interfaccia di legame con Lhcb6, la subunità monomerica che funge da connettore specifico per l’LHCII trimerico di tipo “M”. L'incorporazione di Lhcb4.3 nel supercomplesso PSII-LHCII sembrerebbe svolgere quindi un ruolo importante nel ridurre le dimensioni dell'antenna funzionale, riducendo l’affinità di legame di antenne aggiuntive (tipo “M”) per ridurre l’efficienza di raccolta della luce già ad intensità moderate. L'esposizione ad HL invece, oltre ad indurre la diminuzione dell'antenna del PSII in supercomplessi isolati, determina anche la riduzione parziale di tutte le antenne del PSII presenti nelle membrane tilacoidi, impedendo quindi danni al centro di reazione quando la luce incidente supera costantemente la sua capacità di utilizzarla efficientemente. Questi risultati contribuiscono ad aumentare le conoscenze su come il sistema di antenne associate al PSII è attivamente regolata a lungo termine modulando l’espressione genica in piante acclimatate a diverse intensità di luce.
La flessibilità del sistema modulare di antenne del PSII e la sua interazione strutturale con il centro catalitico, oltre ad essere fondamentale per l’architettura tridimensionale delle membrane tilacoidi delle piante, ha certamente giocato un ruolo chiave nel determinare la loro notevole diversificazione nel corso dell’evoluzione. Nel complesso questi risultati potrebbero fornire nuovi spunti per ampliare la conoscenza di come le associazioni di PSII e LHCII e la loro reciproca interazione contribuiscono a mantenere la complessa architettura delle membrane tilacoidi e quindi l'efficienza complessiva della fotosintesi in condizioni ambientali in continuo mutamento.

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EPrint type:Ph.D. thesis
Tutor:Morosinotto, Tomas
Supervisor:Pagliano, Cristina
Ph.D. course:Ciclo 29 > Corsi 29 > BIOSCIENZE E BIOTECNOLOGIE
Data di deposito della tesi:30 January 2017
Anno di Pubblicazione:30 January 2017
Key Words:Photosystem II, photosynthesis, supercomplex, LHCII, light harvesting, PSII, cryo-EM, structure, light acclimation, SWATH, mass-spectrometry, electron microscopy
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/10 Biochimica
Area 05 - Scienze biologiche > BIO/04 Fisiologia vegetale
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:10133
Depositato il:06 Nov 2017 14:24
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