Johan Decelle

BioStudies – one package for all the data supporting a study

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 supply of photosynthetically derived carbon energy from 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 chloroplast and CO ₂ -fixing pyrenoid of the microalga Micractinium conductrix significantly expands during symbiosis within their host (the ciliate Paramecium bursaria ) compared to the free-living stage. This is accompanied by a threefold higher quantity of Rubisco enzymes, 16-fold higher carbon fixation rate per algal cell and upregulation of several Carbon Concentrating Mechanism-related genes. Time-resolved subcellular quantitative imaging revealed that photosynthetically fixed carbon is first allocated to starch during the day, with five times higher production in symbiosis. Nearly half of the carbon stored in starch is consumed overnight while some is converted into lipid droplets, which are 20-fold more voluminous in symbiotic microalgae. We also show that carbon is transferred to the host and potentially respired by the high density of surrounding host mitochondria. Yet, high starch and lipid content in symbiotic microalgae suggest a moderate carbon export to the host relative to the high primary productivity. Overall, this study provides an original view of the subcellular remodeling and dynamics of carbon metabolism of microalgae inside a host, and opens new questions on the mechanisms of the source–sink relationship in aquatic photosymbiosis.

Radiolaria are unicellular marine organisms (protists) that have been drifting in oceanic plankton for hundreds of millions of years. These mineral architects can build extraordinarily complex skeletons, which fascinated and puzzled naturalists observing water samples through rudimentary microscopes. In the 19th century, the discovery and study of Radiolaria are associated with scientific voyages and human adventures. Naturalists who studied medicine and anatomy in European universities were captivated by the morphology of Radiolaria and expressed a profound wanderlust to collect them in the ocean. These intrepid and workaholic adventurers devoted their restless lives to studying microscopic life, while also actively engaging in teaching and sharing their observations and hypotheses with students. This article aims to retrace the discovery of Radiolaria through the lives of prominent naturalists and marine biologists, primarily Christian Gottfried Ehrenberg, Thomas Henry Huxley, Johannes Müller, and Ernst Haeckel. It also highlights the intellectual and geographic influences that shaped their research, including figures such as Johannes Wolfgang von Goethe and Alexander von Humboldt, as well as places like Jena, Helgoland, Villefranche‐sur‐Mer and Italy, which served as sampling locations and sources of romantic and artistic inspiration. Pioneering work on Radiolaria played a central role in shaping several emerging concepts (e.g., cell theory, individuality) and fields (e.g., taxonomy, evolution of morphology, symbiosis). The discovery of Radiolaria therefore reveals that even the most elusive marine microorganisms can deeply transform our understanding of life.

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 cellular imaging using focused ion beam scanning electron microscopy. Our multiscale 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 as voluminous as those at the shaded base, despite 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.

Phaeocystales, comprising the genus Phaeocystis and an uncharacterized sister lineage, are nanoplanktonic haptophytes widespread in the global ocean. Several species form mucilaginous colonies and influence key biogeochemical cycles, yet their underlying diversity and ecological strategies remain underexplored. Here, we present new genomic data from 13 strains, including three high-quality reference genomes (N50 > 30 kbp), and integrate previous metagenome-assembled genomes to resolve a robust phylogeny. Divergence timing of P. antarctica aligns with Miocene cooling and Southern Ocean isolation. Genomic traits reveal metabolic flexibility, including mixotrophic nitrogen acquisition in temperate waters and gene expansions linked to polar nutrient adaptation. Concordantly, transcriptomic comparisons between temperate and polar Phaeocystis suggest Southern Ocean populations experience iron and B₁₂ limitation. We also identify signatures of horizontal gene transfer and endogenous giant virus/virophage insertions. Together, these findings highlight Phaeocystales as an ecologically versatile and geographically widespread lineage shaped by evolutionary innovation and adaptation to contrasting environmental stressors.

BioStudies – one package for all the data supporting a study

: Symbiosis 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 µm 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 µm/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.

Summary: Symbiosis between eukaryotic microalgae and heterotrophic hosts is a widespread, phylogenetically convergent, and ecologically important phenomenon in aquatic ecosystems. Partners include taxonomically diverse microalgae interacting with multicellular or unicellular hosts in marine or freshwater environments. While progress has been made recently, there are still major knowledge gaps on the microenvironmental conditions of microalgae in hospite (e.g. nutrient and CO₂ availability), the algal carbon metabolism (production and storage), and the cellular mechanisms of carbohydrate export to the host. This review aims to provide current knowledge on the physiology and metabolism of symbiotic microalgae, to highlight whether there are commonalities across different photosymbioses, and to identify new approaches and technologies for disentangling photosymbiotic interactions at relevant temporal and spatial scales.

Summary: Gephyrocapsa huxleyi is a prevalent, bloom‐forming phytoplankton species in the oceans. It exhibits a complex haplodiplontic 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. Here, we investigated the fate of decoupled cells during culture observations and we compared the transcriptome profiles and the cellular ultrastructure of the three life cycle cell types. We found that decoupled cells can revert to the calcified form in the absence of viral pressure, revealing the ability of G. huxleyi to modulate cell differentiation as a function of external conditions. Ultrastructural analyses showed distinct nuclear organization with variations in chromatin volume. Transcriptomic analyses revealed gene expression patterns specific to each life phase. These included multiple regulatory functions in chromatin remodeling, broader epigenetic mechanisms and life cycling, likely contributing to cell differentiation. Finally, analyses of available host–virus transcriptomes support life cycle transition during viral infection. This study provides cellular and molecular foundations for nuclear remodeling and cell differentiation in coccolithophores and the identification of gene markers for studying coccolithophore life cycles in natural populations.