Biology subjects

Decelle, J.

Publications and source records attributed to Decelle, J..

At least 19 recordsLinked to original sources

bioRxiv2026

Diel remodeling and cellular integration of the nitroplast

Nitrogen-fixing eukaryotes were not believed to exist in nature until the recent discovery of a N2-fixing organelle, or nitroplast, in the marine microalga Braarudosphaera bigelowii. This nitroplast (formerly known as UCYN-A2) has long been recognized as key cyanobacterial contributor to global oceanic N2 fixation. However, how this novel organelle is integrated and regulated within the architecture of a eukaryotic cell remains unclear. Here, we combine multiscale volumetric imaging with cryo-electron tomography to resolve the native architecture, cellular integration, and diel remodeling of the nitroplast in cultured and environmental cells. We find that the nitroplast occupies up to 10% of the cell volume and exhibits close interfaces with multiple host organelles through membrane contact sites, while integration of this metabolically demanding compartment does not disrupt global scaling of host organelles. Interestingly, the chloroplast-to-nitroplast volume ratio is conserved across distinct life stages. Cryo-electron tomography reveals that the nitroplast retains a reinforced four-layer cyanobacterial envelope and is additionally surrounded by two host-derived layers that remodel across the day-night cycle. During daytime N2 fixation, these host-derived barriers become locally discontinuous and the organelle interface becomes enriched with two distinct vesicle populations. Our findings suggest that dynamic control of organelle accessibility through transient membrane gating represents a fundamental strategy by which eukaryotic cells could domesticate new endosymbiotic functions during early organellogenesis.

cell biology↗

bioRxiv2026

An Advanced Mobile Laboratory to enable field-based microbial ecology and cell biology across scales

Microbial biodiversity is central to ecosystem function, yet mechanistic insights into the cell biology of environmental organisms remain limited. The underlying challenges are twofold: most microbes remain uncultivable, and a persistent gap exists between field sampling and laboratory analyses. Here, we introduce the Advanced Mobile Laboratory (AML), a field-deployable platform that integrates confocal microscopy, image-enabled cell sorting, and cryo-preparation for expansion and electron microscopy. This setup enables immediate, standardized processing and analysis of environmental communities directly at the sampling site. We demonstrate its capability using marine eukaryotic plankton, showing how the AML enables multiscale investigations, from live imaging of natural communities to enabling ultrastructural and single-cell omics analyses, while minimizing sample degradation and enabling on-site experimentation. By bringing high-end sample preparation and analytical capacity into the field, the AML enables studying life in its natural context to mechanistically understand lifes diversity in the environment.

cell biology↗

bioRxiv2025

Subcellular assessment of algal carbon storage and chloroplasts across the microenvironmental landscape of a photosymbiotic coral

Light availability plays a central role in shaping the photophysiology and energy metabolism of photosymbiotic organisms such as reef-building corals. Although light varies greatly within coral colonies, the effects of this spatial heterogeneity on the subcellular organization and energy storage of symbiotic algae (Symbiodiniaceae) remain poorly understood. Here, we combined microscale measurements of light and oxygen across both light-exposed upper regions and shaded basal regions of a Favites abdita colony with three-dimensional subcellular imaging using Focused Ion Beam Scanning Electron Microscopy (FIB-SEM). Our multi-scale approach revealed subcellular heterogeneity among symbiont populations, suggesting different cell cycle stages and physiological states across a spatial stratification in the coral. Subcellular morphometrics revealed that symbiont cells at the top of the colony were twice more voluminous than those at the shaded base with similar plastid volume occupancy. Compared to symbionts at the top of the colony, symbionts in the basal region accumulated nearly three times more starch relative to their cell volume. These findings show that light gradients within coral colonies shape symbiont morphology and energy storage patterns, with important implications for coral stress tolerance and resilience.

cell biology↗

bioRxiv2025

Long-range actin-driven endosymbiont mobility in a deep-diverging bilaterian

AbstractSymbiosis is everywhere, and "we have never been individuals"[1, 2]. In animal-microbe symbioses, established symbionts are often thought to be confined to a specific cellular or tissue niche[3-7] and generally lose their motile appendages such as flagella[8-15]. However, whether the loss of motile appendages necessarily implies immobility within the animal host remains an open conundrum. Here, we present the discovery of long-range, host actin-driven symbiont mobility in a dinoflagellate-acoel worm symbiosis. Using long-term tracking, fluorescence, and electron microscopy, we find that dinoflagellate symbionts (Amphidinium sp., 10-20{micro}m in size) travel throughout an extensive network of thin host cells ([~]200 nm in regions without symbionts) in Waminoa sp. acoel worms, which are part of a deep-diverging bilaterian lineage[16-18]. Although FIB-SEM-based 3D reconstruction shows symbionts still retain both flagella, we uncover that it is host actin machinery that plays a primary role in overcoming large drag forces under confinement to achieve mobility throughout the worm at surprisingly high velocities (around 1{micro}m/s). Long term in-toto imaging further reveals diel rhythms and spatiotemporal regulation of symbionts during regeneration. Our findings show the presence of host-mediated mobility in animal-microbe symbioses, which suggests the existence of previously overlooked regulatory processes in holobionts maintenance of dynamic homeostasis.

biophysics↗

bioRxiv2025

Two Spore Types in a Marine Parasite of Dinoflagellates

Marine alveolates (MALVs) are diverse, primarily parasitic micro-eukaryotes that significantly impact marine ecosystems. The life cycles of most MALVs remain elusive and the role of sexual reproduction in these organisms is a key question that may determine their ecological success. In this study we focus on a widespread dinoflagellate parasite of bloom-forming dinoflagellates, Amoebophrya. After infection, we identified two distinct spores, differing in size, ultrastructure, swimming behavior, lifespan, gene expression, and metabolite composition. The smaller spores serve as infectious propagules, equipped with an apical complex for host invasion. They exhibit a distinct, shorter, and straighter swimming pattern, likely optimized for an extended lifespan while enhancing dispersion and chance for host encounters. Transcriptomic analysis reveals that these smaller spores are primed for efficient protein synthesis upon initiating a new infection. Conversely, the larger spores cannot infect new hosts and are characterized by the expression of meiotic genes, underscoring their sexual nature. They have a shorter lifespan, exhibit more tortuous movement, along display condensed chromosomes, signaling readiness for mating. Interestingly, infected hosts already express meiotic genes, and a single infected host only produces progeny of the same spore type, suggesting that cell fate is determined prior to spore release. Our study provides one of the first formal demonstrations of a sexually specialized cell in MALVs. Isolating compatible strains for cross-breeding and understanding how environmental conditions favor each reproductive route are the next key questions for elucidating the ecological success of MALVs in marine waters. Significance StatementMarine alveolates (MALVs) are ecologically significant parasites that impact carbon cycling, causing major disease outbreaks affecting fisheries and aquaculture, and influencing the dynamics of harmful algal blooms. Despite their diversity and wide host range, much of our knowledge comes from environmental DNA, leaving important aspects of their biology, such as their life cycles, largely unknown. This study provides the first evidence of sexual reproduction in MALVs, linking spore polymorphism to infective or sexual routes. This discovery is crucial as sexual reproduction increases genetic diversity and adaptability, aiding MALVs resilience in changing environments. Understanding MALVs reproductive strategies deepens our insight into their ecological roles and their broader impact on marine ecosystems.

microbiology↗

bioRxiv2025

The give and take in photosymbiosis unraveled by metabolomics of Radiolaria

Marine planktonic Radiolaria harboring symbiotic microalgae are ubiquitous in the oceans and abundant in oligotrophic areas. In these low-nutrient environments they are among the most important primary producers. Systematic studies of radiolarian biology are limited because Radiolaria are non-culturable and prone to damage during sampling. To obtain insight into the mechanistic basis of radiolarian photosymbiosis we address here the metabolic contributions of the partners to the performance of the holobiont. Therefore, we describe the metabolic inventory of two highly abundant photosymbiotic Radiolaria - colony-forming Collodaria and single-celled Acantharia and compare their metabolomes to metabolomes of respective free-living algae. Most of the metabolites detected in the symbiosis are not present in the free-living algae, suggesting a significant transformation of symbionts metabolites by the host. The metabolites identified in both the holobiont and the free-living algae encompass molecules of primary metabolism and a number of osmolytes, including dimethylsulfoniopropionate. Mass spectrometry imaging revealed the presence of dimethylsulfoniopropionate in both the symbionts and host cells, indicating that the algae provide osmolytic protection to the host. Furthermore, our findings suggest a possible dependence of Collodaria on symbiotic vitamin B3. Distinctive differences in phospholipid composition between free-living and symbiotic stages indicate that the algal cell membrane may undergo rearrangement in the symbiosis. Our results demonstrate a strong interdependence and rewiring of the algal metabolism underlying Radiolaria-microalgae photosymbioses.

microbiology↗

bioRxiv2024

FeatureForest: the power of foundation models, theusability of random forests

Once the work at the microscope is done, biological discoveries rely heavily on proper downstream analysis. This often amounts to first segmenting the biological objects of interest in the image before performing a quantitative analysis. Deep-learning (DL) is nowadays ubiquitous in such segmentation tasks. However, DL can be cumbersome to apply, as it often requires large amount of manual labeling to produce ground-truth data, and expert knowledge to train the models from scratch. Nonetheless, the performance of large foundation models, although trained on natural images, are improving on scientific images with every new model released. They, however, require either manual prompting or tedious post-processing to selectively segment the biological objects of interest. Classical machine learning algorithms, such as random forest classifiers, on the other hand, are well-established, easy to train, and often yield results of sufficient quality for downstream processing tasks, hence their continued popularity. Unfortunately, they are limited to objects with distinct, well-defined textures compared to their environment. This generally limits their usefulness to structures easy to recognize. Here, we present FeatureForest, an open-source tool that leverages the feature embeddings of large foundation models to train a random forest classifier, thereby providing users with a rapid way of semantically segmenting complex images using only a few labeling strokes. We demonstrate the improvement in performance over a variety of datasets, including large and complex volumetric electron microscopy stacks. Our implementation is available in napari, currently integrates four foundation models, and can easily be extended to any new model once they become available.

bioinformatics↗

bioRxiv2024

Hijacking and Integration of Algal Plastids andMitochondria in a Polar Planktonic Host

In oceanic plankton, various host organisms are capable of engulfing and temporarily integrating microalgae (photosymbiosis) or just their photosynthetic plastids (kleptoplastidy) as a solar-powered energy source. These cellular interactions can be considered to be representative of evolutionary steps in plastid acquisition in eukaryotes, but the underlying cellular mechanisms and dynamics are not fully understood. Here, we studied a kleptoplastidic dinoflagellate (RSD: Ross Sea Dinoflagellate), which is known to steal plastids of the microalga Phaeocystis antarctica. We tracked the morphology and activity of stolen plastids over several months by combining multimodal subcellular imaging and photophysiology. Upon integration inside a host vacuole, the volume of plastids and pyrenoids significantly increased and photosynthetic activity was boosted along with carbon fixation and transfer to the host. This may be supported by the retention of a 50-fold larger algal nucleus for [~]1 week. Once the algal nucleus was lost, there was a decrease in plastid volume and photosynthesis, but plastids were still beneficial for the host after > 2 months. Unlike other kleptoplastidic interactions, we showed that the algal mitochondrion was also stolen and retained for several months, transforming into an extensive network in close proximity with plastids. This highlights a new strategy in plankton along the continuum of plastid symbioses where both the energy-producing plastid and mitochondrion of a microalga are hijacked for several months by a host. This symbiosis that we found to be widely-distributed in polar regions suggests that plastid-mitochondrion interaction may have played a role in the evolution of plastid acquisition.

ecology↗

bioRxiv2024

Plastid translocon recycling in dinoflagellates demonstrates the portability of complex plastids between hosts

The plastids of photosynthetic organisms on land are predominantly primary plastids derived from an ancient endosymbiosis of a cyanobacterium. Conversely, marine photosynthetic diversity is dominated by plastids gained by subsequent endosymbioses of photosynthetic eukaryotes, so-called complex plastids. The plastids of major eukaryotic lineages including cryptophytes, haptophytes, stramenopiles, dinoflagellates and apicomplexans, were originally all posited to derive from a single secondary endosymbiosis of a red alga--the chromalveloate hypothesis 1. Subsequent phylogenetic resolution of eukaryotes indicated that separate events of plastid acquisition must have occurred to account for this distribution of plastids 2,3. The number of such events, however, and the donor organisms for the new plastid endosymbioses are still not resolved. A perceived bottleneck of endosymbiotic plastid gain is the development of protein targeting from the hosts into new plastids, and this supposition has often driven hypotheses towards minimising the number of plastid-gain events to explain plastid distribution in eukaryotes. But how plastid protein-targeting is established for new endosymbionts is often unclear, which makes it difficult to assess the likelihood of plastid transfers between lineages. Here we show that Kareniaceae dinoflagellates, that possess complex plastids known to be derived from haptophytes, acquired all the necessary protein import machinery from these haptophytes. Furthermore, cryo-electron tomography revealed that no additional membranes were added to the Kareniaceae complex plastid during serial endosymbiosis, suggesting that the haptophyte-derived import processes were sufficient. Our analyses suggests that complex red plastids are preadapted for horizontal transmission, potentially explaining their widespread distribution in aquatic algal diversity.

evolutionary biology↗

bioRxiv2024

Life Cycle and Morphogenetic Differentiation in Heteromorphic Cell Types of a Cosmopolitan Marine Microalga

O_LIGephyrocapsa huxleyi is a prevalent, bloom-forming phytoplankton species in the oceans. It exhibits a complex haplo-diplontic life cycle, featuring a diploid-calcified phase, a haploid phase, and a third decoupled phase produced during viral infection. Decoupled cells display a haploid-like phenotype, but are diploid. C_LIO_LIHere, we investigated the fate of decoupled cells during culture observations and we compared the transcriptome profiles and the cellular ultrastructure of the three cell types. C_LIO_LIWe found that decoupled cells can revert to the calcified form in the absence of viral pressure, revealing the transient nature of this cell type. Ultrastructural analyses showed distinct nuclear organisation with variations in chromatin volume. Transcriptomic analyses revealed gene expression patterns specific to each life phase. These included multiple regulatory functions in chromatin remodelling, broader epigenetic mechanisms and life cycling, which likely contributed to cell differentiation. Finally, the exploration of available host-virus transcriptomes supports life cycle transition during viral infection. C_LIO_LIThis study provides cellular and molecular foundations for nuclear remodelling and cell differentiation in coccolithophores and the identification of gene markers for studying coccolithophore life cycles in natural populations. C_LI

plant biology↗

bioRxiv2024

Single-cell transcriptomics highlights sexual cues among reproductive life stages of uncultivated Acantharia (Radiolaria)

As an innate property of life, the ability to reproduce is a key process for the perpetuation of organisms. Along the evolution of protist reproductive strategies, the molecular machinery of sexual recombination is estimated to have been inherited from the last eukaryotic common ancestor (LECA). Nevertheless, unraveling the sexual cycles of extant free-living protist lineages remains challenging, given the enigmatic roles of many uncultivated life stages. Among the uncultivated planktonic group of Acantharia (Radiolaria), a hypothetical sexual cycle has been proposed since the late 19th century, including the existence of a gamete-like life stage of undetermined ploidy, referred to as swarmers. In order to investigate the sexual nature of acantharian reproductive stages, we conducted single-cell transcriptomic analysis across various acantharian life stages. Our results show distinct functional profiles for reproductive and vegetative life stages, while revealing the expression of the reference eukaryotic genes involved in gamete fusion, HAP2/GCS1 and GEX1-KAR5, in swarmers and pre-swarmer stages. Annotation of differentially expressed life stage-specific genes, also highlights putative meiosis-related functions among swarmers, while suggesting the existence of a potential swarmer/vegetative intermediate stage expressing putative growth-related genes. This original life stage-specific genetic data is coherent with morphological evidence supporting the existence of an acantharian sexual cycle, with swarmers acting as gametes. Moreover, it paves the way for a deeper understanding of radiolarian cell biology and ecology at a single-cell scale. HighlightsO_LIAcantharia demonstrate both morphological and genetic evidence of a sexual cycle C_LIO_LIAcantharian reproductive stages are enriched in functions related to cell division C_LIO_LINuclear fusion gene family GEX1-KAR5 is up-regulated in putative acantharian gametes C_LIO_LIMost expressed genes specific to acantharian reproductive stages are unassigned C_LIO_LIReproduction-specific unassigned genes include putative sex-related functions C_LI

microbiology↗

bioRxiv2024

Transportome remodeling of a symbiotic microalga inside a planktonic host

Metabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic host and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Yet, the identity of transferred carbohydrates as well as the molecular mechanisms that drive this exchange remain largely unknown, especially in unicellular photosymbioses that are widespread in the open ocean. Combining genomics, single-holobiont transcriptomics and environmental metatranscriptomics, we revealed the transportome of the marine microalga Phaeocystis in symbiosis within acantharia, with a focus on sugar transporters. At the genomic level, the sugar transportome of Phaeocystis is comparable to non-symbiotic haptophytes. By contrast, we found significant remodeling of the expression of the transportome in symbiotic microalgae compared to the free-living stage. More particularly, 32% of sugar transporter genes were differentially expressed. Several of them, such as GLUTs, TPTs and aquaporins, with glucose, triose-phosphate sugars and glycerol as potential substrates, were upregulated at the holobiont and community level. We also showed that algal sugar transporter genes exhibit distinct temporal expression patterns during the day. This reprogrammed transportome indicates that symbiosis has a major impact on sugar fluxes within and outside the algal cell, and highlights the complexity and the dynamics of metabolic exchanges between partners. This study improves our understanding of the molecular players of the metabolic connectivity underlying the ecological success of planktonic photosymbiosis and paves the way for more studies on transporters across photosymbiotic models.

cell biology↗

bioRxiv2023

Sweet and fatty symbionts: photosynthetic productivity and carbon storage boosted in microalgae within a host

Symbiosis between a host and intracellular eukaryotic microalgae is a widespread life strategy in aquatic ecosystems. This partnership is considered to be mainly energized by the photosynthetically-derived carbon energy of microalgal symbionts. A major question is whether microalgae increase their photosynthetic production and decrease carbon storage in order to maximize carbon translocation to their host. By combining three-dimensional subcellular imaging and physiological analyses, we show that the photosynthetic machinery (chloroplast and CO2-fixing pyrenoid) of the symbiotic microalga Micractinium conductrix significantly expands inside their host (the ciliate Paramecium bursaria) compared to the free-living state. This is accompanied by a 13-fold higher quantity of Rubisco enzymes and 16-fold higher carbon fixation rate. Time-resolved subcellular imaging revealed that photosynthetically-derived carbon is first allocated to starch during the day, with five times higher production in symbiosis despite low growth. Nearly half of the carbon stored in starch is consumed overnight and some accumulates in lipid droplets, which are 20-fold more voluminous in symbiotic microalgae. We also show that carbon is transferred to the host and hypothesize that much of this is respired by the high density of surrounding host mitochondria. We provide evidence that the boosted photosynthetic production of symbiotic microalgae could be explained by the energetic demands of the host. Overall, this study provides an unprecedented view of the subcellular remodeling and dynamics of carbon metabolism of microalgae inside a host, highlighting the potentially key role of the source-sink relationship in aquatic photosymbiosis. Significance statementSymbiotic interactions between a heterotrophic host and intracellular microalgae are widespread in aquatic ecosystems and are considered to be energized by the photosynthetically-derived carbon energy. However, little is known on the impact of symbiosis on the algal bioenergetics (e.g. carbon production and storage). This study reveals the morphological and physiological changes of a microalga inside a host at the subcellular scale over the day. We show that the photosynthetic machinery expands and carbon fixation and storage are boosted in symbiotic microalgae beyond their growth needs. This high photosynthetic production is very likely enhanced by the host energetic demands. Our findings advance our basic understanding of photosymbiosis and open new perspectives on the mechanisms and drivers of metabolic exchange between partners.

physiology↗

bioRxiv2023

Targeted volume Correlative Light and Electron Microscopy of an environmental marine microorganism

Photosynthetic microalgae are responsible for an important fraction of CO2 fixation and O2 production on Earth. Three-dimensional ultrastructural characterization of these organisms in their natural environment can contribute to a deeper understanding of their cell biology. However, the low throughput of volume electron microscopy (vEM) methods, along with the complexity and heterogeneity of environmental samples, pose great technical challenges. In the present study, we used a workflow based on a specific EM sample preparation, compatible with both light and vEM imaging in order to target one cell among a complex natural community. This method revealed the 3D subcellular landscape of a photosynthetic dinoflagellate with quantitative characterization of multiple organelles. We could show that this cell contains a single convoluted chloroplast and the arrangement of the flagellar apparatus with its associated photosensitive elements. Moreover, we observed chromatin features that could shed light on how transcriptional activity takes place in organisms where chromosomes are permanently condensed. Together with providing insights in dinoflagellates biology, this proof-of-principle study illustrates an efficient tool for the targeted ultrastructural analysis of environmental microorganisms in heterogeneous mixes.

cell biology↗

bioRxiv2022

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↗

bioRxiv2021

Intracellular development and impact of a eukaryotic parasite on its zombified microalgal host in the marine plankton

Parasites are widespread and diverse in the oceanic plankton, and many of them infect single-celled algae for survival. How these parasites develop and scavenge energy within the host and whether the cellular organization and metabolism of the host is altered remain open questions. Combining quantitative structural and chemical imaging with time-resolved transcriptomics, we unveil dramatic morphological and metabolic changes of the parasite Amoebophrya (Syndiniales) during intracellular infection (e.g. 200-fold increase of mitochondrion volume), particularly following digestion of nutrient-rich host chromosomes. Some of these changes are also found in the apicomplexan parasites (e.g. sequential acristate and cristate mitochondrion, switch from glycolysis to TCA), thus underlining key evolutionary-conserved mechanisms. In the algal host, energy-producing organelles (chloroplast) remain intact during most of the infection, but sugar reserves diminish while lipid droplets increase. Thus, rapid infection of the host nucleus could be a zombifying strategy to digest nutrient-rich chromosomes and escape cytoplasmic defense while benefiting from the maintained C-energy production of the host cell.

cell biology↗

bioRxiv2021

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↗

bioRxiv2020

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↗