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Toullec, G.

Publications and source records attributed to Toullec, G..

5 recordsLinked to original sources

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↗

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↗

Symbiotic nutrient exchange enhances the long-term survival of cassiosomes, the autonomous stinging-cell structures of Cassiopea

Medusae of the widely distributed and locally invasive upside-down jellyfish Cassiopea release autonomous, mobile stinging structures. These so-called cassiosomes are a major contributor to contactless stinging incidents in (sub-)tropical shallow waters. While the presence of endosymbiotic dinoflagellates in cassiosomes has previously been observed, their potential contribution to the metabolism and long-term survival of cassiosomes is unknown. Combining stable isotope labeling and correlative SEM and NanoSIMS imaging with a long-term in vitro experiment, this study reveals a mutualistic symbiosis based on nutritional exchanges in dinoflagellate-bearing cassiosomes. We were able to show that organic carbon input from the dinoflagellates fuels the metabolism of the host tissue and enables anabolic nitrogen assimilation. Thanks to this symbiotic nutrient exchange, cassiosomes showed enhanced survival in the light compared to dark conditions for at least one month in vitro. Overall, this study demonstrates that cassiosomes, in analogy with Cassiopea medusae, are photosymbiotic holobionts. Cassiosomes thus promise to be a powerful new miniaturized model system for in-depth ultrastructural and molecular investigation of cnidarian photosymbioses.

ecology↗

Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis

Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was to a large extent concealed by body shrinkage of the starving animals, resulting in what could be referred to as invisible bleaching. Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in our warming oceans.

ecology↗

Comparative population genomics provide new insight into the evolutionary history and adaptive potential of World Ocean krill

AbstractGenetic variation is instrumental for adaptation to new or changing environments but it is poorly understood how it is structured and contributes to adaptation in pelagic species without clear barriers to gene flow. Here we use extensive transcriptome datasets from 20 krill species collected across the Atlantic, Indian, Pacific and Southern Oceans and compare genetic variation both within and between species across thousands of genes. We resolve phylogenetic interrelationships and uncover genomic evidence in support of elevating the cryptic Euphausia similis var. armata into species. We estimate levels of genetic variation and rates of adaptive protein evolution among species and find that these are comparably low in large Southern Ocean species endemic to cold environments, including the Antarctic krill Euphausia superba, suggesting their adaptive potential to rapid climate change may also be low. We uncover hundreds of candidate loci with signatures of adaptive divergence between krill native to cold and warm waters and identify candidates for cold-adaptation that have also been detected in Antarctic fish, including genes that govern thermal reception such as TrpA1. Our results suggest parallel genetic responses to similar selection pressures across Antarctic taxa and provide new insights into the adaptive potential of important zooplankton that are already strongly affected by climate change.

evolutionary biology↗