Biology subjects

Yee, D. P.

Publications and source records attributed to Yee, D. P..

5 recordsLinked to original sources

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↗

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

A proton pump enhancing photosynthesis links phagocytosis to marine phytoplankton symbiogenesis

Diatoms, dinoflagellates, and coccolithophorids are the dominant groups of marine eukaryotic phytoplankton collectively responsible for the majority of primary production in the ocean1. These phytoplankton contain additional intracellular membranes around their chloroplasts derived from ancestral engulfment of red microalgae by unicellular heterotrophic eukaryotes that led to secondary endosymbiosis2. This symbiogenesis hypothesis for the origin of modern secondary endosymbiotic phytoplankton is supported by a wealth of palaeontologic, morphologic, and genomic evidence3-6. However, the selectable evolutionary advantage of these membranes and the physiological significance for extant phytoplankton are unknown. We report that the proton-pumping enzyme V-type H+-ATPase (VHA), ubiquitously used in eukaryotic intercellular digestion, is localized around the chloroplasts of centric diatoms and that VHA-activity significantly enhances photosynthesis over a wide range of oceanic irradiances. Similar results in pennate diatoms, dinoflagellates, and coccolithophorids, but not green or red microalgae, imply a mechanism resulting from the co-option of phagocytic VHA activity into a carbon concentrating mechanism that is common to secondary endosymbiotic phytoplankton. Furthermore, analogous VHA-dependent mechanisms in extant photosymbiotic marine invertebrates7-9 provide functional evidence for an adaptive advantage throughout the transition from endosymbiosis to symbiogenesis. Our results suggest that VHA-dependent enhancement of photosynthesis contributes at least 7% of primary production in the ocean, providing an example of a symbiosis-derived evolutionary innovation with global environmental implications.

evolutionary biology↗

bioRxiv2020

Enhanced triacylglycerol (TAG) and protein accumulation in transgenic diatom Thalassiosira pseudonana with altered photosynthetic pigmentation

Microalgal productivity in mass cultures is limited by the inefficiency with which available light energy is utilized. In dense cultures, cells closest to the light source absorb more light energy than they can use and dissipate the excess, while light penetrance into the culture is steeply attenuated. Reducing microalgal light harvesting and/or dissipating capacity per cell may improve total light utilization efficiency in mass cultures. In this study, two transgenic lines of the diatom Thalassiosira pseudonana with altered photosynthetic pigment content are evaluated with respect to photosynthetic parameters, growth, and macromolecule accumulation. In one line, violaxanthin de-epoxidase-like 2 (VDL2) is overexpressed (OE), resulting in a reduction of the diadinoxanthin cycle pigments, which are involved in light energy dissipation (non-photochemical quenching, NPQ), accompanied by a stoichiometric increase in the light-harvesting pigment fucoxanthin. No differences in the maximum potential quantum yield of photosystem II (Fv/Fm) or light-limited photosynthetic rate () were found. However, when adapted to 30 {micro}mol photons m-2 sec-1, the VDL2 OE maximum relative electron transport rate (rETRmax) upon exposure to saturating light intensities was 86-95% of wild type (WT). When adapted to 300 {micro}mol photons m-2 sec-1, VDL2 OE saturated photosynthesis at 62-71% of the light intensity needed to saturate WT (Ek). NPQ was substantially lower at and below 300 {micro}mol photons m-2 sec-1. VDL2 OE accumulated up to 3.4 times as much triacylglycerol (TAG) as WT during exponential growth, and up to twice as much protein. Growth in terms of culture density was up to 7% slower. TAG and protein accumulation inversely correlated with NPQ. The second line evaluated was obtained by using antisense RNA to simultaneously silence or knock down (KD) both LUT1-like (LTL) genes, hypothesized to catalyze an intermediate carotenoid biosynthesis step of converting {beta}-carotene to zeaxanthin. Overall reduction of photosynthetic pigment content without altering the relative abundance of individual pigments resulted. No significant differences in photosynthetic parameters compared to WT were found. LTL KD grew at a rate comparable to WT and accumulated up to 40% more TAG during exponential growth, while protein content was reduced by 11-19%. LTL KD cells were elongated and 5-10% smaller than WT, and cultures contained auxospores, indicating stress that may relate to a cell cycle progression defect.

microbiology↗