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Finazzi, G.

Publications and source records attributed to Finazzi, G..

16 recordsLinked to original sources

Thylakoid plasticity primes photoprotection in diatoms

For many millions of years, diatoms have been major primary producers in marine ecosystems, supporting food webs and contributing to carbon sequestration through the export of photosynthetically fixed carbon to the deep ocean, mitigating atmospheric carbon dioxide levels and global climate. A key factor in their ecological success is their ability to rapidly adapt to fluctuating light, balancing efficient light harvesting under dim conditions with energy dissipation under excess light. However, the mechanisms behind this regulation have not been fully elucidated. This study shows that several processes contribute to dissipating excess excitation energy in diatoms exposed to light stress: (i) the detachment of the oxygen-evolving complex proteins from the PSII core, leading to energy dissipation via charge recombination, (ii) Non-Photochemical Quenching (NPQ) in the antenna, i.e., thermal dissipation of excited states and (iii) excitation energy transfer from PSII to PSI via energy spillover. The latter process is observed in parallel with high light-induced topological changes of the thylakoids that may favor transient interactions between the photosystems. Along with the accumulation of light-stress-protecting carotenoids on longer time-scales, this ensemble of photoprotective mechanisms provides a dynamic and flexible response to the light challenges expected in coastal marine habitats.

biochemistry↗

MorphoLearn: A morphology-driven workflow to decipher 3D electron microscopy segmentation in diatoms

Three-dimensional electron microscopy (3D EM) enables the quantitative analysis of cellular ultrastructure. However, large-scale segmentation of whole-cell volumes poses a significant challenge, especially in biologically diverse systems. Unlike medical and animal cell imaging, which often benefit from temporal redundancy and relatively uniform morphology, studies of microbial and microalgal biodiversity must rely on static snapshots. These snapshots exhibit high variability in cell shape, organelle organisation, and image contrast. Consequently, robust AI-assisted segmentation in this context requires models that learn directly from morphological features and can adapt to heterogeneous sample preparation. In this paper, we present a systematic framework for AI-assisted segmentation of Focused Ion Beam-Scanning Electron Microscopy (FIB-SEM) datasets. This framework is specifically designed to address the challenges posed by morphological diversity and contrast variability while remaining within realistic computational constraints. We evaluate multiple lightweight 3D encoder-decoder architectures and identify VNet as the best option for balancing computational efficiency and volumetric accuracy in whole-cell segmentation. Using datasets from two strains of Phaeodactylum tricornutum and extending our analysis to cross-species comparisons, we demonstrate that training on specific regions of interest can lead to an overestimation of model performance. In contrast, performing whole-cell segmentation uncovers significant differences in architectural robustness. Moreover, we show that transfer learning and contrast-aware hybrid strategies allow for efficient adaptation to previously unseen datasets with minimal annotation. The incorporation of boundary-aware loss functions significantly enhances the delineation of closely associated organelles, such as chloroplasts and mitochondria, in multi-class segmentation tasks. Together, these findings establish a scalable, reproducible, and biologically informed AI framework for 3D FIB-SEM segmentation. This framework enables high-throughput analysis of cellular ultrastructure across diverse species and imaging conditions. Author SummaryCells exhibit a wide range of shapes, sizes, and internal structures, particularly among various microbial species. These morphological differences are not arbitrary; they indicate how cells adapt to their environments and manage essential biological functions. Modern three-dimensional electron microscopy can capture this structural diversity at the nanometre scale, but analysing the resulting data is often slow. This is due to the time-consuming process of manually outlining cellular structures, which also requires expert knowledge. Artificial intelligence (AI) has made significant advances in accelerating image analysis in medical and animal cell studies, typically by learning from repeated observations over time. However, studies focusing on microbial and microalgal biodiversity often rely on single snapshots of diverse cells prepared under varying imaging conditions. This complicates automated analysis since AI systems must learn from morphology directly rather than from temporal repetition. In this study, we developed and evaluated an AI-assisted segmentation framework specifically for whole-cell 3D electron microscopy data. By systematically comparing efficient neural network architectures and incorporating transfer learning and contrast-aware strategies, we demonstrate that accurate segmentation can be achieved even with limited training data and standard computing resources. Our approach facilitates faster, scalable, and reproducible analysis of cellular ultrastructure, paving the way for large-scale investigations into cell morphology, adaptation, and diversity across species. Significance statementQuantitative analysis of cellular ultrastructure across species is currently limited by challenges in segmenting large three-dimensional electron microscopy datasets. Unlike medical imaging, which often benefits from artificial intelligence due to its use of temporal repetition and consistent morphology, studies of microbial biodiversity depend on single snapshots that display extreme variations in cell shape and image contrast. This work presents a scalable, morphology-driven AI framework for whole-cell 3D segmentation that is resilient to biological diversity and variations in sample preparation. By enabling accurate analysis with minimal annotations and standard computational resources, this approach enhances access to high-throughput ultrastructural studies and facilitates comparative investigations of cellular adaptation across different species.

cell biology↗

Chloroplast-mitochondria synergy modulates responses to iron limitation in two Thalassiosira diatom species

Iron is naturally present at low levels in modern oceans, but it remains essential for marine life. Ocean-dwelling organisms such as oceanic phytoplankton must therefore adapt to the available levels. Among phytoplankton, diatoms are a highly diverse and successful taxon that includes the Thalassiosira genus. As a group, diatoms contribute around 20% of global primary photosynthetic productivity, they have also developed specific resources allowing them to thrive in low-iron regions. However, the major biological factors underlying their success in these ocean environments remain unknown. Here, we compared two Thalassiosira species: T. oceanica from iron-poor open-ocean; and T. pseudonana, from iron-rich coastal waters. Since iron is essential for both photosynthesis and respiration, we examined the specificities of the bioenergetic machineries in these organisms using a combination of photo-physiological, proteomics, and FIB-SEM methods. We particularly focused on chloroplast-mitochondrial coupling, a mechanism deployed by diatoms to ensure optimal transfer of photosynthetic products to promote cell growth. This study of this mechanism in the context of iron limitation reveals that the two diatoms differentially remodel chloroplast compartments in response to iron limitation. Their tolerance to these conditions is also linked to distinct constitutive mitochondrial architectures.

plant biology↗

Deciphering Photosynthetic Protein Networks: A Crosslinking-MS Strategy for Studying Functional Thylakoid Membranes

Photosynthesis, which sustains life on Earth, depends on organized and yet adaptable protein assemblies embedded in specialized membranes known as thylakoids. Understanding how these complexes interact and reorganize within functional photosynthetic membranes is essential to reveal the molecular basis of energy conversion in cells. Here, we present an improved crosslinking mass spectrometry strategy that captures native protein interactions in photosynthetically active thylakoid membranes from Arabidopsis thaliana and Spinacia oleracea. By monitoring photosynthetic performance during crosslinking, we show that electron transport remains active, allowing structural analysis under physiological conditions. Moreover, we show that trimethylphenylammonium chloride (TMPAC) as an adjuvant charged compound does not impair physiological activity, while boosting and diversifying crosslink identifications. Mapping crosslinks onto known structures confirms the integrity of major photosynthetic complexes and uncovers previously uncharacterized assemblies involving regulatory and structural proteins. Integration with structural modeling and interaction network analysis identifies novel protein players within the photosynthetic machinery, providing molecular insights into their potential roles. This approach offers a broadly applicable framework for studying membrane protein organization and dynamics in functional bioenergetic systems. Significance StatementPhotosynthesis relies on dynamic protein interactions within thylakoid membranes, yet capturing these networks under physiological conditions remains challenging. We establish a crosslinking mass spectrometry workflow that maps native protein interactions in plant thylakoids while preserving photosynthetic activity. By bridging structural and functional biology, this approach enables in situ exploration of membrane protein networks and advances our understanding of photosynthetic regulation

plant biology↗

A genome-wide CRISPR screen reveals how diatoms thrive in dynamic light

Diatoms are a highly diverse group of phytoplankton that have a large impact on global primary production and carbon sequestration in the ocean1,2. However, they are evolutionarily divergent from model phototrophs of the green lineage, and limited screening tools have hampered discovery of unique diatom biology. To address this challenge, we developed a genome-wide CRISPR/Cas9 screen in the model marine diatom, Phaeodactylum tricornutum. The screen was applied to identify genes required for survival in different light regimes, including both high light and fluctuating light. We identified a broad set of uncharacterized genes, providing the foundation for mechanistic studies of diatom adaptation to dynamic light. Among these genes, we demonstrated that the red lineage-exclusive gene STROBE1 is a new potentiator of cyclic electron flow (CEF) required for CEF to generate a trans-thylakoid proton gradient3,4. As dynamic light conditions are common in marine environments, STROBE1 and other genes identified in this screen may contribute to the broad ecological success of diatoms5,6. This genome-wide genetic screen in P. tricornutum will accelerate the unbiased discovery of novel gene functions in these ecologically important organisms.

microbiology↗

Photoreceptor-induced LHL4 protects photosystem II in Chlamydomonas reinhardtii

Photosynthesis, the fundamental process using light energy to convert CO2 to organic matter, is vital for life on Earth. It relies on capturing light through light-harvesting complexes in evolutionarily well-conserved photosystems (PS) I and II and on the conversion of light energy into chemical energy. Composition and organization of both photosystem core complexes are well conserved across evolution. PSII is particularly sensitive to photodamage but benefits from a large diversity of photoprotective mechanisms, finely tuned for the specific light conditions. Light Harvesting Complex protein family members (LHC and LHC-like families) have acquired a dual function during evolution. Members of the LHC antenna complexes of photosystems capture light energy whereas others dissipate excess energy that cannot be harnessed for photosynthesis. This process mainly occurs through non photochemical quenching (NPQ). In this work, we focus on the LHL4 protein, which is a LHC-like protein induced by UV-B and blue light photoreceptor signaling pathways in the model green microalgae Chlamydomonas reinhardtii. We demonstrate that alongside established NPQ effectors, LHL4 plays a key role in photoprotection, preventing singlet oxygen accumulation in PSII and promoting cell survival upon light stress. LHL4 protective function is distinct from that of NPQ-related proteins, as it specifically and uniquely binds to the transient monomeric form of the core PSII complex, safeguarding its integrity. LHL4 characterization expands our understanding of the interplay between light harvesting and photoprotection mechanisms upon light stress in photosynthetic microalgae.

plant biology↗

Deciphering lipid mutant phenotypes with a new genome-scale metabolic model of Microchloropsis gaditana encompassing detailed lipid metabolism

The oleaginous microalga Microchloropsis gaditana (formerly Nannochloropsis gaditana) has gained large interest due to its potential to produce lipids for a wide range of biotechnological applications. To optimize M. gaditana growth conditions and develop new strains to enhance lipid synthesis and accumulation, a broad understanding of the organism metabolism is essential. Computational models such as genome-scale metabolic models constitute powerful tools for unravelling microorganism metabolism. In this work we present iMgadit23, a new genome-scale metabolic model for M. gaditana. Model covers 2330 reactions involving 1977 metabolites and associated with 889 genes. Pathways involved in membrane and storage glycerolipid biosynthesis and degradation have undergone thorough manual curation and have been comprehensively described based on current knowledge of M. gaditana lipid metabolism. Additionally, we developed a detailed 2D-pathway map of model content to provide a systems-level visualization of M. gaditana metabolism. We demonstrated the predictive capabilities of iMgadit23, validating its ability to qualitatively and quantitatively capture in vivo growth phenotypes under diverse environmental and genetic conditions. Model was also able to capture the role of the Bubblegum acyl-CoA synthetase in remodeling M. gaditana lipid metabolism. iMgadit23 and its 2D map constitute valuable tools to increase understanding of M. gaditana metabolism and deciphering mutant phenotypes, specifically in the context of lipid metabolism. The model holds significant promise in predicting M. gaditana metabolic capabilities, facilitating strain engineering, and optimizing cultivation processes for a broad range of industrial applications.

plant biology↗

Diatom pyrenoids are encased in a protein shell that enables efficient CO2 fixation

Pyrenoids are subcompartments of algal chloroplasts that concentrate Rubisco enzymes and their CO2 substrate, thereby increasing the efficiency of carbon fixation. Diatoms perform up to 20% of global CO2 fixation, but their pyrenoids remain poorly characterized at a molecular level. Here, we used in vivo photo-crosslinking to catalogue components of diatom pyrenoids and identified a pyrenoid shell (PyShell) protein, which we localized to the pyrenoid periphery of both the pennate diatom, Pheaodactylum tricornutum, and the centric diatom, Thalassiosira pseudonana. In situ cryo-electron tomography (cryo-ET) revealed that the pyrenoids of both diatom species are encased in a lattice-like protein sheath. Disruption of PyShell expression in T. pseudonana resulted in the absence of this protein sheath, altered pyrenoid morphology, and a high-CO2 requiring phenotype, with impaired growth and reduced carbon fixation efficiency under standard atmospheric conditions. Pyrenoids in mutant cells were fragmented and lacked the thylakoid membranes that normally traverse the Rubisco matrix, demonstrating how the PyShell plays a guiding role in establishing pyrenoid architecture. Recombinant PyShell proteins self-assembled into helical tubes, enabling us to determine a 3.0 [A]-resolution PyShell structure. We then fit this in vitro structure into an in situ subtomogram average of the pyrenoids protein sheath, yielding a putative atomic model of the PyShell within diatom cells. The structure and function of the diatom PyShell provides a new molecular view of how CO2 is assimilated in the ocean, a crucial biome that is on the front lines of climate change.

cell biology↗

Tailoring confocal microscopy for in-cell photophysiology studies

Photoautotrophs environmental responses have been extensively studied at the organism and ecosystem level. However, less is known about their photosynthesis at the single cell level. This information is needed to understand photosynthetic acclimation processes, as light changes as it penetrates cells, layers of cells or organs. Furthermore, cells within the same tissue may behave differently, being at different developmental/physiological stages. Here we describe a new approach for single-cell and subcellular photophysiology based on the customisation of confocal microscopy to assess chlorophyll fluorescence quenching by the saturation pulse method. We exploit this setup to: i. reassess the specialisation of photosynthetic activities in developing tissues of non-vascular plants; ii. identify a specific subpopulation of phytoplankton cells in marine photosymbiosis, which are consolidating metabolic connections with their animal hosts, and iii. testify to the link between light penetration and photoprotection responses inside the different tissues that constitute a plant leaf anatomy. MotivationVisualising photosynthetic responses in 3D is essential for understanding most acclimation processes, as light changes within photosynthetic tissues as it penetrates the absorbing/diffusing layers of the cells. To achieve this goal, we developed a new imaging workflow merging confocal microscopy and saturating pulse chlorophyll fluorescence detection. This method applies to samples characterised by increasing complexity and its simplicity will contribute to its widespread use in plant and microalgae photoacclimation studies.

plant biology↗

Photosynthetic light harvesting and thylakoid organization in a CRISPR/Cas9 Arabidopsis thaliana LHCB1 knockout mutant.

Light absorbed by chlorophylls of photosystem II and I drives oxygenic photosynthesis. Light-harvesting complexes increase the absorption cross-section of these photosystems. Furthermore, these complexes play a central role in photoprotection by dissipating the excess of absorbed light energy in an inducible and regulated fashion. In higher plants, the main light-harvesting complex is the trimeric LHCII. In this work, we used CRISPR/Cas9 to knockout the five genes encoding LHCB1, which is the major component of the trimeric LHCII. In absence of LHCB1 the accumulation of the other LHCII isoforms was only slightly increased, thereby resulting in chlorophyll loss leading to a pale green phenotype and growth delay. Photosystem II absorption cross-section was smaller while photosystem I absorption cross-section was unaffected. This altered the chlorophyll repartition between the two photosystems, favoring photosystem I excitation. The equilibrium of the photosynthetic electron transport was partially maintained by a lower photosystem I over photosystem II reaction center ratio and by the dephosphorylation of LHCII and photosystem II. Loss of LHCB1 altered the thylakoid structure, with less membrane layers per grana stack and reduced grana width. Stable LHCB1 knock out lines allow characterizing the role of this protein in light harvesting and acclimation and pave the way for future in vivo mutational analyses of LHCII.

plant biology↗

Photoprotection is regulated by light-independent CO2 availability

Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO2 conditions. When light energy exceeds CO2 fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO2 Concentrating Mechanism (CCM). How light and CO2 signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO2 concentrations and that depletion of CO2 drives these responses, even in total darkness. High CO2 levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3/CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO2 and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO2 levels.

plant biology↗

Impaired photoprotection in Phaeodactylum tricornutum KEA3 mutants reveals the proton regulatory circuit of diatoms light acclimation.

Diatoms are amongst the most successful clades of oceanic phytoplankton, significantly contributing to photosynthesis on Earth. Their ecological success likely stems from their ability to acclimate to changing environmental conditions, including e.g. variable light intensity. Diatoms are outstanding at dissipating light energy exceeding the maximum photosynthetic electron transfer (PET) capacity of via Non Photochemical Quenching (NPQ). While the molecular effectors of this process, as well as the role of the Proton Motive Force (PMF) in its regulation are known, the putative regulators of the PET/PMF relationship in diatoms remain unidentified. Here, we demonstrate that the H+/K+ antiporter KEA3 is the main regulator of the coupling between PMF and PET in the model diatom Phaeodactylum tricornutum. By controlling the PMF, it modulates NPQ responses at the onset of illumination, during transients and in steady state conditions. Under intermittent light KEA3 absence results in reduced fitness. Using a parsimonious model including only two components, KEA3 and the diadinoxanthin de-epoxidase, we can describe most of the feedback loops observed between PET and NPQ. This two-components regulatory system allows for efficient responses to fast (minutes) or slow (e.g. diel) changes in light environment, thanks to the presence of a regulatory Ca2+-binding domain in KEA3 that controls its activity. This circuit is likely finely tuned by the NPQ effector proteins LHCX, providing diatoms with the required flexibility to thrive in different ocean provinces. One sentence summaryThe author(s) responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plcell/pages/General-Instructions) is Giovanni Finazzi.

plant biology↗

Subcellular architecture and metabolic connection in the planktonic photosymbiosis between Collodaria (radiolarians) and their microalgae

Photosymbiosis is widespread and ecologically important in the oceanic plankton but remains poorly studied. Here, we used multimodal subcellular imaging to investigate the photosymbiosis between colonial Collodaria and their microalga dinoflagellate (Brandtodinium) collected in surface seawaters. We showed that this symbiosis is a very dynamic system whereby symbionts interact with different host cells via extracellular vesicles within the "greenhouse-like" colony. 3D electron microscopy revealed that the volume of the photosynthetic apparatus (plastid and pyrenoid) of the microalgae increased in symbiosis compared to free-living while the mitochondria volume was similar. Stable isotope probing coupled with NanoSIMS showed that carbon and nitrogen were assimilated and stored in the symbiotic microalga in starch granules and purine crystals, respectively. Nitrogen was also allocated to the algal nucleus (nucleolus). After 3 hours, low 13C and 15N transfer was detected in the host Golgi. Metal mapping revealed that intracellular iron concentration was similar in free-living and symbiotic microalgae (ca 40 ppm) and two-fold higher in the host, whereas copper concentration increased in symbiotic microalgae (up to 6900 ppm) and was detected in the host cell and extracellular vesicles. Sulfur mapping also pinpointed the importance of this nutrient for the algal metabolism. This study, which revealed subcellular changes of the morphology and nutrient homeostasis in symbiotic microalgae, improves our understanding on the metabolism of this widespread and abundant oceanic symbiosis and paves the way for more studies to investigate the metabolites exchanged.

ecology↗

Cytoklepty in the plankton: a host strategy to optimize the bioenergetic machinery of endosymbiotic algae

Endosymbioses have shaped the evolutionary trajectory of life and remain widespread and ecologically important. Investigating modern oceanic photosymbioses can illuminate how algal endosymbionts are energetically exploited by their heterotrophic hosts, and inform on putative initial steps of plastid acquisition in eukaryotes. By combining 3D subcellular imaging with photophysiology, carbon flux imaging and transcriptomics, we show that cell division of algal endosymbionts (Phaeocystis) is blocked within hosts (Acantharia), and that their cellular architecture and bioenergetic machinery are radically altered. Transcriptional evidence indicates that a nutrient-independent mechanism prevents symbiont cell division and decouples nuclear and plastid division. As endosymbiont plastids proliferate, the volume of the photosynthetic machinery volume increases 100-fold in correlation with expansion of a reticular mitochondrial network in close proximity to plastids. Photosynthetic efficiency tends to increase with cell size and photon propagation modeling indicates that the networked mitochondrial architecture enhances light capture. This is accompanied by 150-fold higher carbon uptake and upregulation of genes involved in photosynthesis and carbon fixation, which, in conjunction with a ca.15-fold size increase of pyrenoids demonstrates enhanced primary production in symbiosis. NanoSIMS analysis revealed major carbon allocation to plastids and transfer to the host cell. Invagination of the symbiosome into endosymbionts to optimize metabolic exchanges is strong evidence that the algal metamorphosis is irreversible. Hosts therefore trigger and unambiguously benefit from major bioenergetic remodeling of symbiotic microalgae with important consequences for the oceanic carbon cycle. Unlike other photosymbioses, this interaction represents a so-called cytoklepty, which is a putative initial step towards plastid acquisition.

physiology↗

In-cell quantitative structural imaging of phytoplankton using 3D electron microscopy

Phytoplankton is a minor fraction of the global biomass playing a major role in primary production and climate. Despite improved understanding of phytoplankton diversity and genomics, we lack nanoscale subcellular imaging approaches to understand their physiology and cell biology. Here, we present a complete Focused Ion Beam - Scanning Electron Microscopy (FIB-SEM) workflow (from sample preparation to image processing) to generate nanometric 3D phytoplankton models. Tomograms of entire cells, representatives of six ecologically-successful phytoplankton unicellular eukaryotes, were used for quantitative morphometric analysis. Besides lineage-specific cellular architectures, we observed common features related to cellular energy management: i) conserved cell-volume fractions occupied by the different organelles; ii) consistent plastid-mitochondria interactions, iii) constant volumetric ratios in these energy-producing organelles. We revealed detailed subcellular features related to chromatin organization and to biomineralization. Overall, this approach opens new perspectives to study phytoplankton acclimation responses to abiotic and biotic factors at a relevant biological scale.

plant biology↗

Identification of the Calmodulin-dependent NAD+ kinase sustaining the elicitor-induced oxidative burst in plants

NADP(H) is an essential cofactor ofmultiple metabolic processes in all living organisms. While NADP+ production in plants has long been known to involve a Calmodulin (CaM)/Ca2+-dependent NAD+ kinase, the nature of the enzyme catalyzing this activity has remained enigmatic, as well as its role in plant physiology. Here, we identify an Arabidopsis P-loop ATPase (Atlg04280) with a bacterial type II zeta toxin domain, that catalyzes NADP+ production upon binding of CaM/Ca2+ to a domain located in its N-terminal region. The encoded protein (NADKc-1) is associated with the mitochondria and amplifies the elicitor-induced oxidative burst in Arabidopsis leaves representing the missing link between calcium signalling and metabolism in the response to pathogen elicitor. By analysis of various plants and algae, we show that NADKc is well conserved in the plant lineage and present in basal plants. Our data allows proposing that the CaM-dependent NAD kinase activity is only found in photosynthetic species carrying NADKc-1 related proteins, which would represent the only proteins harboring CaM-dependent NAD kinase activity in plants and algae.

plant biology↗