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Meneghesso, Andrea (2016) Investigation of mechanisms modulating photosynthetic efficiency in Nannochloropsis gaditana. [Ph.D. thesis]

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Abstract (english)

Oxygenic photosynthesis is a crucial process for life on earth as it enables plants and algae to convert sunlight into chemical energy, generating molecular oxygen as a byproduct. Light can also be harmful and when in excess can drive to photosystems over‐excitation and production of reactive oxygen species (ROS) with the consequent decrease of the overall photosynthetic efficiency. In a highly dynamic natural environment photosynthetic organisms have evolved sophisticated mechanisms to modulate their efficiency to capture and exploit light. For instance the so called non photochemical quenching of fluorescence (NPQ) acts dissipating excess energy as heat and it’s used as short term response to high light in order to avoid oxidative damages. The carotenoid zeaxanthin belonging to the xanthophyll cycle enhances this thermal dissipation but also has a direct role in the scavenging of ROS generated in the membrane. Acclimation instead is a more complex long term process that acts directly modeling the composition of the photosynthetic apparatus in response to different light intensity, for example through modifications in protein composition. Photoregulation and photoprotection are strongly related also to modulations of flow of excitation energy and electrons across the thylakoid membrane. Indeed the major pathway for the light reactions of photosynthesis, the linear electron flow, can modulate its rate depending on metabolic demand and can be also supported by alternative electron pathway which affect the thylakoid gradient across the membrane and the ATP/NADPH ratio.
The general aim of this work is to investigate the different mechanisms modulating photosynthetic efficiency in the microalga Nannochloropsis gaditana in order to increase the limited knowledge about this interesting microalga and exploit it to optimize photosynthetic efficiency in a large-scale cultivation perspective, even through the development of computational models. The spectroscopic tools developed to untangle the complexity of the photosynthetic regulation in Nannochloropsis have been successfully applied to study photosynthesis in other photosynthetic organisms such as, Chlamydomonas reinhardtii, Physcomitrella patens and Koliella antarctica.
Nannochloropsis gaditana is an eukaryotic alga of the phylum of heterokonta, originating from a secondary endosymbiotic event. Species of this group have received increasing attention in the scientific community, reflecting their potential application in biofuel production, although the photosynthetic and physiological properties of these organisms remain poorly characterized. Nannochloropsis species have a peculiar photosynthetic apparatus characterized by the presence of chlorophyll a, violaxanthin and vaucheriaxanthin as the most abundant pigments.
The regulation of the photosynthetic apparatus in this interesting microalgae has been deeply discussed in Section B. Our study focused firstly on the acclimation response in Nannochloropsis gaditana subjected to prolonged exposition to low and high light. Intense illumination induces a decrease in the chlorophyll content and the antenna size of both Photosystem I and II. Cells grown in high light also show increased photosynthetic electron transport, paralleled by an increased contribution of cyclic electron transport around Photosystem I. Even when exposed to extreme light intensities, Nannochloropsis cells do not activate photo-protection responses, such as NPQ and the xanthophyll cycle in a constitutive way. Conversely, these responses remained available for activation upon additional changes in illumination. These results suggest NPQ and the xanthophyll cycle in Nannochloropsis gaditana play exclusive roles in response to short-term changes in illumination but only play a slight role, if any, in responses to chronic light stress.
In order to further explore the short term response mediated by xanthophyll cycle the effect of zeaxanthin accumulation in the photosynthetic apparatus of Nannochloropsis gaditana was investigated revealing some peculiar aspects. Interestingly zeaxanthin molecules are found to be constitutively present in this microalga, even in conditions of very low light in which the xanthophyll cycle is not yet induced. In addition this xanthophyll does not show a specific binding site in the different protein components of the photosynthetic apparatus and, in addition, has a strong effect in the NPQ response. The influence on NPQ seems to be related mostly on de novo synthesis of zeaxanthin while the molecules already present in the photosynthetic apparatus are involved in a transient NPQ active only in the first minute after the dark-light transition.
The regulation of the photosynthetic apparatus has been assessed also in N. salina in a growing system more compatible with a large-scale production system, a continuous-flow flat-plate photobioreactor. Interestingly changing the residence time maintaining the same irradiation affects the biomass concentration leading to an acclimation response very similar to that observed for N. gaditana grown in batch system, as previously discussed. These results highlight the importance of the biomass concentration and its connection with light supply as parameter to optimize in order to increase the microalgal culture productivity.
The molecular investigation of the mechanisms at the basis of light exploitations in Nannochloropsis is the starting point for the development of computational models that aim to simulate and predict microalgae behavior in order to optimize their productivity in large-scale cultivation systems. Section C deals with the development and widespread application of these models, which integrate chlorophyll fluorescence measurements allowing also the representation of complex mechanisms such as NPQ. Such models prove especially useful in identifying which parameters have the largest impact on productivity, thereby providing a means for enhancing growth through design and operational changes. They can also provide guidance for genetic engineering by identifying those modifications having the largest potential impact on productivity.
In Section D the study of photosynthetic processes is expanded to other organisms focusing on the regulation of the photosynthetic electron chain through the employment of several spectroscopic approaches set up during my PhD thesis. In the first work reported we show that the introduction of a mitochondrial mutation in Chlamydomonas reinhardtii mutants depleted in the chloroplastic PGRL1 rescue its photosensitivity in high light. Detailed functional analysis of these cells showed that the mitochondria mutation alters the electron transport reactions increasing alternative electron pathways around PSI at the detriment of PSII-related photosynthesis. This work thus clearly shows how mitochondrial activity play a seminal influence on photosynthesis in algae.
The second work presented deals with another important mechanisms to modulate flow of excitation, the Mehler-like reactions mediated by Flavodiiron (FLV) proteins. These proteins were lost during evolution of land plants but are still present in non vascular plants, as the moss Physcomitrella patens, the model organism employed for this study. P. patens mutants depleted in FLV show these proteins are active as an electron sink downstream of Photosystem I. Measurement of electron transport showed that they play a major role particularly in the first seconds after a sudden change in light intensity, when for a few seconds they are the major sink for electrons from PSI. When exposed to fluctuating light FLV mutants showed light sensitivity and PSI photoinhibition, demonstrating their biological role as a safety valve for excess electrons in dynamic light. FLV absence in mutants was, in part, compensated by increased cyclic electron flow, suggesting that their biological role may have been substituted in vascular plants by this other mechanism of alternative electron flow.
Finally we analyzed the time course of physiological and morphological responses to different irradiances in Koliella antarctica, a green antarctic microalga isolated from Ross Sea. K. antarctica not only modulates cell morphology and composition of its photosynthetic apparatus on a long-term acclimation, but also shows the ability of a very fast response to light fluctuations. The ability to activate such responses is fundamental for survival in its natural extreme environment.

Abstract (italian)

La fotosintesi ossigenica è un processo fondamentale per la vita sulla terra in quanto consente a piante e alghe di convertire la luce solare in energia chimica generando ossigeno molecolare come sottoprodotto. La luce può anche essere dannosa e quando è in eccesso può portare alla sovreccitazione dei fotosistemi e alla produzione di specie reattive dell'ossigeno (ROS) con un conseguente calo dell’efficienza fotosintetica. In un ambiente naturale estremamente dinamico gli organismi fotosintetici hanno evoluto meccanismi sofisticati in grado di modulare la loro efficienza per catturare e sfruttare al meglio la luce. Per esempio il cosiddetto quenching non fotochimico della fluorescenza (NPQ) agisce dissipando l’energia in eccesso sotto forma di calore ed è utilizzato come sistema di risposta a breve termine agi stress luminosi col fine di evitare danni ossidativi. Il carotenoide zeaxantina appartenente al ciclo delle xantofille partecipa attivamente a questa risposta di dissipazione termica mantenendo però anche un ruolo diretto nello scavenging dei ROS generati nella membrana tilacoidale. L’acclimatazione invece è un processo a lungo termine che agisce direttamente modellando la composizione dell'apparato fotosintetico in risposta all'intensità della luce ad esempio attraverso modifiche nella composizione proteica. I meccanismi di regolazione e protezione indotti dalla luce sono spesso legati anche a modulazioni dei flussi elettronici attraverso la membrana tilacoidale. La via principale per le reazioni alla luce della fotosintesi infatti, il flusso elettronico lineare, è in grado di modulare la sua attività a seconda della richiesta metabolica e può essere sostenuto anche da pathways elettronici alternativi che influenzano il gradiente tilacoidale e il rapporto ATP / NADPH.
L'obiettivo generale di questo lavoro è quello di indagare i diversi meccanismi che modulano l'efficienza fotosintetica nella microalga Nannochloropsis gaditana al fine di aumentare la conoscenza ancora limitata di questa microalga e sfruttarla per ottimizzare l'efficienza fotosintetica in un ottica di coltivazione su larga scala, anche attraverso lo sviluppo modelli di calcolo. Gli strumenti spettroscopici sviluppati per districare la complessità dei meccanismi di regolazione della fotosintesi in Nannochloropsis sono stati applicati con successo anche per lo studio di altri organismi fotosintetici quali, Chlamydomonas reinhardtii, Physcomitrella patens e Koliella antarctica.
Nannochloropsis gaditana è un'alga eucariotica del phylum heterokonts originata da un evento di endosimbiosi secondaria. Specie di questo gruppo hanno ricevuto una crescente attenzione nella comunità scientifica che riflette la loro potenziale applicazione nella produzione di biocarburanti. Nonostante questo le proprietà fotosintetici e fisiologiche di questi organismi rimangono ancora poco caratterizzate. La specie Nannochloropsis possiede un apparato fotosintetico peculiare contenente come pigmenti più abbondanti clorofilla a, violaxantina e vaucheriaxantina. La regolazione dell'apparato fotosintetico in questa microalga è stato approfondito nella Sezione B. Il nostro studio si è concentrato in primo luogo sulla risposta di acclimatazione in Nannochloropsis gaditana sottoposta a prolungate esposizioni a luce bassa e alta. L’illuminazione intensa induce una diminuzione del contenuto di clorofilla e delle dimensioni della taglia d’antenna del PSI e II. Cellule coltivate in alta luce mostrano anche un aumento del trasporto fotosintetico degli elettroni di pari passo con un maggior contributo da parte del trasporto alternativo ciclico. Anche quando esposte a intensità di luce estreme, le cellule di Nannochloropsis non attivano le risposte di foto-protezione, come ad esempio NPQ e il ciclo delle xantofille, in modo costitutivo. Al contrario, queste risposte rimangono a disposizione per l'attivazione in risposta a ulteriori modifiche dell’ illuminazione. Questi risultati suggeriscono che l’NPQ e il ciclo delle xantofille in Nannochloropsis gaditana giocano un ruolo esclusivo in risposta alle variazioni luminose a breve termine, ma solo un ruolo marginale nelle risposte al stress luminosi cronico.
Al fine di esplorare ulteriormente la risposta a breve termine mediata dal ciclo delle xantofille è stato studiato l'effetto dell’ accumulo di zeaxantina nell'apparato fotosintetico di Nannochloropsis gaditana rivelando alcuni aspetti peculiari. E’ interessante notare che le molecole di zeaxantina si trovano ad essere sintetizzate costitutivamente in questa microalga, anche in condizioni di scarsa illuminazione in cui il ciclo delle xantofille non viene indotto. Inoltre questa xantofilla ha dimostrato di non avere un sito di legame specifico nelle diverse componenti proteiche dell’apparato fotosintetico e ha in aggiunta un forte effetto nella risposta di NPQ. L’effetto legato all’ NPQ sembra legato principalmente alla sintesi de novo di zeaxantina mentre le molecole già presenti nel’apparato fotosintetico sono coinvolte in un NPQ transitorio attivo solo nel primo minuto dopo la transizione luce-buio.
La regolazione dell'apparato fotosintetico è stata valutata anche in N. salina in un sistema di coltivazione più compatibile con la produzione su larga scala, un fotobioreattore a flusso continuo. È interessante notare che modificare il tempo di permanenza mantenendo la stessa irradiazione influisce sulla concentrazione di biomassa e produce una risposta di acclimatazione molto simile a quella osservata in N. gaditana coltivata in sistema a batch, come precedentemente discusso. Questi risultati evidenziano l'importanza della concentrazione della biomassa e la sua connessione con la luce somministrata come parametro da ottimizzare per aumentare la produttività delle colture microalgali.
L'indagine molecolare sui meccanismi alla base dell’utilizzo della luce in Nannochloropsis è il punto di partenza per lo sviluppo di modelli computazionali che mirano a simulare e prevedere il comportamento delle microalghe nell’ottica di ottimizzare la produttività in sistemi di coltivazione su larga scala. La Sezione C tratta dello sviluppo e dell'applicazione di questi modelli, che integrano misure di fluorescenza della clorofilla e consentono anche la rappresentazione di meccanismi complessi come l’NPQ. Tali modelli risultano particolarmente utili per identificare i parametri che hanno il maggiore impatto sulla produttività algale fornendo inoltre una guida per individuare quelle modifiche genetiche che hanno il maggiore potenziale impatto sulla produttività.
Nella sezione D lo studio dei processi fotosintetici si espande ad altri organismi focalizzandosi in particolare sui meccanismi di regolazione della catena fotosintetica di trasposto degli elettroni. Questo studio si avvale dell'impiego di diverse tecniche spettroscopiche che ho messo a punto durante la mia tesi di dottorato. Nel primo lavoro riportato viene mostrato come l'introduzione di una mutazione mitocondriale nella microalga Chlamydomonas reinhardtii priva della proteina cloroplastica PGRL1 porti ad un recupero delle performance di crescita in condizioni di alta luce. Analisi fotosintetiche effettuate in queste cellule mutanti ha mostrato che la mutazione mitocondriale altera le reazioni di trasporto degli elettroni aumentando i pathways elettronici alternativi che coinvolgono il PSI e limitando fortemente l’attività del PSII. Questo lavoro dimostra come l'attività mitocondriale abbia un'influenza fondamentale sulla fotosintesi delle microalghe.
Il secondo lavoro presentato si occupa di un importante meccanismo volto a modulare il flusso di eccitazione, le reazioni Mehler-like mediate dalle proteine Flavodiiron (FLV). Queste proteine sono state perse durante l'evoluzione delle piante terrestri, ma sono ancora presenti nelle piante non vascolari, come nel muschio Physcomitrella patens, l'organismo modello utilizzato per questo studio. Mutanti di P. patens deprivati della proteina FLV mostrano come quest’ultima abbia un ruolo di sink degli elettroni a valle del PSI. Misure di trasporto elettronico hanno dimostrato che le FLV svolgono un ruolo importante in particolare nei primi secondi dopo una rapida variazione dell'intensità luminosa, quando per alcuni secondi essi agiscono da principale sink degli elettroni provenienti dal PSI. Quando esposti ad una condizione di luce fluttuante i mutanti FLV mostrano fotosensibilità e inibizione del PSI, dimostrando il loro ruolo biologico come valvola di sicurezza in caso di sovrariduzione della catena fotosintetica. L’assenza delle FLV nei mutanti è in parte compensata da un aumento del flusso ciclico degli elettroni, suggerendo che quest’ultimo possa avere sostituito il ruolo biologico delle FLV nelle piante vascolari.
Infine abbiamo analizzato l'andamento nel tempo delle risposte fisiologiche e morfologiche a diverse intensità luminose in Koliella antarctica, una microalga verde antartica isolata nel Mare di Ross. K. antarctica modula non solo la morfologia cellulare e il suo apparato fotosintetico tramite una risposta acclimatativa a lungo termine, ma mostra anche la capacità di rispondere rapidamente alle variazioni dell’intensità luminosa. La possibilità di attivare tali risposte è fondamentale per la sopravvivenza nel suo ambiente naturale estremo.

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EPrint type:Ph.D. thesis
Tutor:Morosinotto, Tomas
Data di deposito della tesi:01 February 2016
Anno di Pubblicazione:01 February 2016
Key Words:Nannochloropsis gaditana, Photosynthetic efficiency, Electrochromic shift (ECS), biofuels, Chlamydomonas reinhardtii, Physcomitrella patens, photoregulation, photoprotection
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:9542
Depositato il:20 Oct 2016 09:33
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