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Dorrell, R. G.

Publications and source records attributed to Dorrell, R. G..

11 recordsLinked to original sources

Chaos and repetition in algal evolution: A Chrysophyceae eco-genomic framework

The Chrysophyceae are an algal class that, within relatively short evolutionary distances, have repeatedly adopted multiple trophic strategies (photoautotrophy, mixotrophy, heterotrophy) and are ubiquitous across marine, freshwater and cryosphere ecosystems. Historical understanding of marine chrysophytes has lagged behind that of freshwater taxa, limiting our ability to identify what genes determine their cellular and ecosystem function. We leverage new transcriptomes, meta-genomes and computational predictions to reveal the functional, genetic and eco-physiological diversity of Chrysophyceae, including newly documented marine groups. We show that their common ancestor was likely a marine mixotroph, with multiple independent colonizations of freshwater and cryospheres, and evolution of photoautotrophic and heterotrophic life-strategies. We identify characteristic biogeographical distributions for different Chrysophyceae orders, including new ones linking marine and freshwater cryospheres. We document convergent gene losses relating to cryotolerance, photosynthesis, and phagocytosis, including novel families widely spread across the algal tree of life. We map meta-gene distributions of marker genes and impute a latitudinal shift in Chrysophyceae trophic strategy, with photoautotrophy predominant in polar oceans and heterotrophy in oligotrophic tropical waters. Our study identifies new gene markers that may be determinant of lifestyle shifts across the algal tree of life and reveals probable responses of marine chrysophytes to climate change.

evolutionary biology↗

Characterisation of the new microalgal protein xATPA related to the F-type ATP synthase α subunit, from the ecosystem to the molecule

Microalgal metabolism relies on their chloroplasts, and involves both nucleus and plastidial-encoded proteins of various evolutionary origins. The plastidial ATP synthase complex is a key player in photosynthesis, and has been extensively studied in plants. However, our knowledge in other photosynthetic eukaryotes remains limited, despite their importance in marine environments. Here, we report the characterisation of a novel homologue of the F-type ATP synthase alpha subunit, hereby named xATPA, widespread in microalgae but absent from other photosynthetic organisms. Comparisons of xATPA sequences and predicted structures revealed a specific feature, the bump domain, and highlighted the absence of an ATP-binding site. We assessed xATPA prevalence in microalgae in the global ocean using environmental data from Tara Oceans, with a particular focus on diatoms, and demonstrate that its expression is associated with polar summer conditions. Using a reverse genetic approach in the model diatom Phaeodactylum tricornutum, we show that xATPAPt has a plastidial localisation, and that xATPA KO mutants exhibit growth deficiencies in a combination of low temperature, low salinity and constant light, consistent with environmental analysis. Surprisingly, both RNAseq and physiological assays suggest that xATPA is not involved in ATP synthase functions. On the other hand, xATPA interacts with other F1 ATP synthase subunits in vitro, which we suggest forms transient unassembled complexes. This study hence represents a comprehensive analysis of a novel protein from the environment to the lab, and reveals a new player in the plastidial physiology of eukaryotic microalgae.

plant biology↗

Dynamic relocalization and divergent expression of a major facilitator carrier subfamily in diatoms

Eukaryotic organisms, including microbial members such as protists and green algae, utilise suites of transporter proteins to move essential metabolites across cell organelle membranes. Amongst these different transporter families, the MCF (Mitochondrial Carrier Family) is one of the most diverse, encompassing essential NAD+ and ADP/ ATP translocators, as well as amino acid, sugar and cofactor transporters. They are typically associated with the mitochondrial inner membrane but some display more dynamic localization. Here, we perform a brief census of MCF domains in the genome of the model diatom alga Phaeodactylum tricornutum, identifying a new family of three proteins (termed here and elsewhere "MCFc") with strong internal sequence conservation but limited similarity to other MCF proteins. Considering both phylogenetic data and experimental localization, we posit that MCFc is widespread across algae with complex red chloroplasts alongside some primary green algae, and contains multiple sub-families targeted to diatom mitochondria, plastids, and endomembranes. Finally, using data from Tara Oceans, we identify putative roles for MCFc in diatom cells, including a probable association of the plastid-targeted Phatr3_J46742 sub-family in cellular nitrate assimilation. Our data provide insights into the evolutionary diversification of the membrane transport mechanisms associated with diatoms and other eukaryotic algae.

cell biology↗

DiatOmicBase, a gene-centered platform to mine functional omics data across diatom genomes

Diatoms are prominent microalgae found in all aquatic environments. Over the last 20 years, thanks to the availability of genomic and genetic resources, diatom species such as Phaeodactylum tricornutum have emerged as valuable experimental model systems for exploring topics ranging from evolution to cell biology, (eco)physiology and biotechnology. Since the first genome sequencing in 2008, numerous genome-enabled datasets have been generated, based on RNA-Seq and proteomics, epigenomes, and ecotype variant analysis. Unfortunately, these resources, generated by various laboratories, are often in disparate formats and challenging to access and analyze. Here we present DiatOmicBase, a genome portal gathering comprehensive omics resources from P. tricornutum and two other diatoms to facilitate the exploration of dispersed public datasets and the design of new experiments based on the prior-art. DiatOmicBase provides gene annotations, transcriptomic profiles and a genome browser with ecotype variants, histone and methylation marks, transposable elements, non-coding RNAs, and read densities from RNA-Seq experiments. We developed a semi-automatically updated transcriptomic module to explore both publicly available RNA-Seq experiments and users private datasets. Using gene-level expression data, users can perform exploratory data analysis, differential expression, pathway analysis, biclustering, and co-expression network analysis. Users can create heatmaps to visualize precomputed comparisons for selected gene subsets. Automatic access to other bioinformatic resources and tools for diatom comparative and functional genomics is also provided. Focusing on the resources currently centralized for P. tricornutum, we showcase several examples of how DiatOmicBase strengthens molecular research on diatoms, making these organisms accessible to a broad research community. Significance statementIn recent years, diatoms have become the subject of increasing interest because of their ecological importance and their biotechnological potential for natural products such as pigments and polyunsaturated fatty acids. Here, we present an interactive web-based server that integrates public diatom omics data (genomics, transcriptomics, epigenomics, proteomics, sequence variants) to connect individual diatom genes to broader-scale functional processes.

genomics↗

Environmentally-informed functional characterization of a plastid diatom metabolic bridge of mitochondrial origin

Withdrawal statementThe authors have withdrawn this manuscript due to a duplicate posting of manuscript number BIORXIV/2022/507166. Therefore, the authors do not wish this work to be cited as reference for the project. If you have any questions, please contact the corresponding author. The correct preprint can be found at doi: 10.1101/2022.09.08.507166

evolutionary biology↗

Presence of vitamin B12 metabolism in the last common ancestor of land plants

Vitamin B12, or cobalamin, (hereinafter B12) is an essential organic micronutrient, required by humans as a cofactor for methionine synthase (METH) and for methylmalonyl CoA mutase (MCM), involved in the propionate shunt. B12 is a complex corrinoid molecule made only by a subset of bacteria. Plants and fungi have an alternative methionine synthase (METE) that does not need a B12 cofactor, so these organisms are typically considered to neither synthesise nor utilise B12. In contrast many algal species utilise B12 if it is available, because they encode both METE and METH. Moreover, a large proportion of algal species encode METH only, and so are like animals in being dependent on an external source of the vitamin. Here, we performed a detailed phylogenetic analysis of the distribution of METE, METH and eleven further proteins implicated in B12 metabolism in eukaryotic cells across an exhaustive library of over 1,500 plant and algal genomes and transcriptomes. The results reveal the hitherto undetected existence of B12-associated metabolism deep into the streptophytes. The B12-dependent synthase METH, and the accessory proteins MTRR, CblB, CblC, CblD and CblJ were detected in the basally divergent plant lineage of hornworts, and CblB and CblJ were further identified in liverworts. Using phylogenetic and PFAM analysis we demonstrate this is due to retention of ancestral B12-metabolism pathways in the last common ancestor of land plants, followed by at least two independent complete losses in mosses and vascular plants. We further show more limited distributions of genes encoding B12-related proteins across the algal tree of life, including MCM and type II ribonucleotide reductase, alongside an obligate B12-dependency across several major marine algal orders. Finally, by considering the functional biology of early-diverging land plants, together with the collection sites of ten further algal species inferred to have lost B12-dependent metabolism, we propose freshwater-to-land transitions and symbiotic associations to have been major constraining factors in B12 availability in early plant evolution.

plant biology↗

Divergent and diversified proteome content across a serially acquired plastid lineage

Dinoflagellates are a diverse group of ecologically significant micro-eukaryotes, prone to the loss and replacement of their plastids via serial endosymbiosis. One such replacement took place in the ancestors of the Kareniaceae, which harbor haptophyte-derived plastids containing the pigment fucoxanthin, instead of the ancestral peridinin dinoflagellate plastid. The metabolic functions of the fucoxanthin plastid are performed by a diverse range of nucleus-encoded and plastid-targeted proteins, which may originate from the haptophyte ancestor of the fucoxanthin plastid, the peridinin-containing ancestor of the dinoflagellate host, and/or from lateral gene transfers. However, the evolutionary composition of fucoxanthin plastid proteomes across the diversity of kareniacean dinoflagellates remains poorly understood. Here, we determine the total composition of the plastid proteomes of seven distantly-related kareniacean dinoflagellates, including newly-sequenced members of three genera (Karenia, Karlodinium, and Takayama). Using a custom plastid-targeting predictor, automatic single-gene tree building and phylogenetic sorting of plastid-targeted proteins, we project relatively limited (~10%) and functionally distinctive contributions of the haptophyte endosymbiont to the fucoxanthin plastid proteome, in comparison to plastid-targeted proteins of dinoflagellate host origin. Considering a concatenated multigene phylogeny of haptophyte-derived plastid proteins, we show that the haptophyte order Chrysochromulinales is the closest living relative of the fucoxanthin plastid donor. We additionally perform detailed analyses of the N-terminal targeting sequences of kareniacean plastid signal peptides, reporting a surprisingly high sequence conservation. Finally, considering planetary-scale distributions of key kareniacean genera and haptophyte orders from Tara Oceans, we suggest ecological and mechanistic factors accompanying the endosymbiotic acquisition of the fucoxanthin plastid.

microbiology↗

A Plastidial Glycolytic-Gluconeogenic Switch of Mitochondrial Origin Enables Diatom Adaptations to High Latitudes

Organic carbon fixed in chloroplasts through the Calvin Cycle can be diverted towards different metabolic fates, including cytoplasmic and mitochondrial respiration; gluconeogenesis; and synthesis of diverse plastid metabolites via the pyruvate hub. In plants, pyruvate is principally produced via cytoplasmic glycolysis, although a plastid-targeted lower glycolytic pathway is known in non-photosynthetic tissue. Here, we characterize a lower plastid glycolytic-gluconeogenesis pathway in diatoms, ecologically important marine algae distantly related to plants. We show that two reversible enzymes required to complete diatom plastid glycolysis-gluconeogenesis, Enolase and PGAM (bis- phospho-glycerate mutase), originated through duplications of mitochondria-targeted respiratory isoforms. Through CRISPR-Cas9 mutagenesis, integrative omic analyses, and measured kinetics of expressed enzymes in the diatom Phaeodactylum tricornutum, we present evidence that this pathway diverts plastid glyceraldehyde-3-phosphate into the pyruvate hub, and may also function in the gluconeogenic direction. Considering experimental data, we show that this pathway has different roles dependent in particular on day length and environmental temperature, and show that it is expressed at elevated levels in high latitude oceans where diatoms are abundant. Our data provide evolutionary, meta-genomic and functional insights into a poorly understood yet evolutionarily recurrent plastid metabolic pathway.

plant biology↗

Dynamic Cell Imaging: application to the diatom Phaeodactylum tricornutum under environmental stresses

The dynamic movement of cell organelles is an important and poorly understood component of cellular organisation and metabolism. In this work we present a non-invasive non-destructive method (Dynamic Cell Imaging, DCI) based on light scattering and interferometry to monitor dynamic events within photosynthetic cells using the diatom Phaeodactylum tricornutum as a model system. For this monitoring we acquire few seconds movies of the signals that are related to the motion of dynamic structures within the cell (denoted scatterers), followed by a statistical analysis of each pixel time series. Illuminating P.tricornutum with LEDs of different wavelengths associated to short pulsed or continuous-wave modes of illumination revealed that dynamic movements depend on chloroplast activity, in agreement with the reduction in the number of pixels with dynamic behaviour after addition of photosystemII inhibitors. We studied P. tricornutum under two environmentally relevant stresses, iron and phosphate deficiency. The major dynamic sites were located within lipid droplets and chloroplast envelope membranes. By comparing standard deviation and cumulative sum analysis of the time series, we showed that within the droplets two types of scatterer movement could be observed: random motions (Brownian type) but also anomalous movements corresponding to a drift which may relate to molecular fluxes within a cell. The method appears valuable for studying the effects of various environments on a large variety of microalgae in the laboratory as well as in natural aquatic environments. HIGHLIGHTsLight scattering an alternative to fluorescence to rapidly evidence dynamic processes. Lipid droplets the major metabolic active sites under stress A non-destructive visualisation method for laboratory microalgae and aquatic samples.. SIGNIFICANCE STATEMENTLight scattering could be an alternative to fluorescence techniques to study dynamic processes within photosynthetic cells. We used a method combining light scattering and interferometry to analyse movements of intracellular scatterers in the marine diatom Phaedactylum tricornutum under two environmentally relevant stresses, iron and phosphate deficiency. Lipid droplets were the major active sites under stress. The method which is rapid and non destructive can be broadly expanded to study other microalgae and their stress responses, in the laboratory and in aquatic environments.

microbiology↗

Within-Arctic horizontal gene transfer as a driver of convergent evolution in distantly related microalgae

The Arctic Ocean is being impacted by warming temperatures, increasing freshwater and highly variable ice conditions. The microalgal communities underpinning Arctic marine food webs, once thought to be dominated by diatoms, include a phylogenetically diverse range of small algal species, whose biology remains poorly understood. Here, we present genome sequences of a cryptomonad, a haptophyte, a chrysophyte, and a pelagophyte, isolated from the Arctic water column and ice. Comparing protein family distributions and sequence similarity across a densely-sampled set of algal genomes and transcriptomes, we note striking convergences in the biology of distantly related small Arctic algae, compared to non-Arctic relatives; although this convergence is largely exclusive of Arctic diatoms. Using high-throughput phylogenetic approaches, incorporating environmental sequence data from Tara Oceans, we demonstrate that this convergence was partly explained by horizontal gene transfers (HGT) between Arctic species, in over at least 30 other discrete gene families, and most notably in ice-binding domains (IBD). These Arctic-specific genes have been repeatedly transferred between Arctic algae, and are independent of equivalent HGTs in the Antarctic Southern Ocean. Our data provide insights into the specialized Arctic marine microbiome, and underlines the role of geographically-limited HGT as a driver of environmental adaptation in eukaryotic algae.

evolutionary biology↗

Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum functional genome and evolutionary origin of diatoms

Diatoms are one of the most successful and ecologically important groups of eukaryotic phytoplankton in the modern ocean. Deciphering their genomes is a key step towards better understanding of their biological innovations, evolutionary origins, and ecological underpinnings. Here, we have used 90 RNA-Seq datasets from different growth conditions combined with published expressed sequence tags and protein sequences from multiple taxa to explore the genome of the model diatom Phaeodactylum tricornutum, and introduce 1,489 novel genes. The new annotation additionally permitted the discovery for the first time of extensive alternative splicing (AS) in diatoms, including intron retention and exon skipping which increases the diversity of transcripts to regulate gene expression in response to nutrient limitations. In addition, we have used up-to-date reference sequence libraries to dissect the taxonomic origins of diatom genomes. We show that the P. tricornutum genome is replete in lineage-specific genes, with up to 47% of the gene models present only possessing orthologues in other stramenopile groups. Finally, we have performed a comprehensive de novo annotation of repetitive elements showing novel classes of TEs such as SINE, MITE, LINE and TRIM/LARD. This work provides a solid foundation for future studies of diatom gene function, evolution and ecology.

bioinformatics↗