Biogeographical Patterns and Genomes of Aquatic Photoautotrophs

Karlusich, Juan José Pierella; Nef, Charlotte; Bowler, Chris; Dorrell, Richard G.

doi:10.1002/9781119986782.ch3

Cited by 4 publications

(3 citation statements)

References 160 publications

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“…S12 ; Supplemental Dataset S 3, sheet 11) (Delmont, Gaia et al 2022). We emphasise these results are preliminary, as many of these genomes are incomplete, and gene non-detection does not formally confirm absence (Delmont, Gaia et al 2022, Pierella Karlusich, Nef et al 2023). For each sMAG, we considered presence or absence of possible plastid-targeted Enolase and PGAM sequences; taxonomic assignation of the MAG; and mean mapped vertical coverage of each MAG in each station (i.e., depth and breadth of the coverage of sequences recruited to each genome), as a proxy for abundance, regardless of whether the plastid-targeted glycolysis genes associated with each sMAG were detected ( Fig.…”

Section: Resultsmentioning

confidence: 77%

Complementary environmental analysis and functional characterization of a plastid diatom lower glycolytic-gluconeogenesis pathway

Dorrell

Liang

Guéguen

et al. 2022

Preprint

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Organic carbon fixed through the Calvin Cycle can be diverted towards different metabolic fates within and beyond the plastids of photosynthetic eukaryotes. These include export to the cytoplasm and mitochondrial respiration; gluconeogenesis of storage compounds; and the anabolic synthesis of lipids, amino acids and cofactors via the plastidial pyruvate hub. In plants, pyruvate is principally synthesised via the lower half of glycolysis-gluconeogenesis in the cytoplasm, although a secondary plastid-targeted pathway in non-photosynthetic tissue directly links glyceraldehyde-3-phosphate to the pyruvate hub. Here, we characterize a complete plastidial lower half glycolytic-gluconeogenic pathway in the photosynthetic plastids of diatoms, obligately photosynthetic eukaryotic algae that are important contributors to marine primary production. We show that the two enzymes required to complete plastidial glycolysis-gluconeogenesis, plastidial Enolase and PGAM (bis-phospho-glycerate mutase), originated through recent duplications of mitochondria-targeted respiratory glycolytic isoforms. Through CRISPR-Cas9 mutagenesis and integrative omic analyses in the diatom Phaeodactylum tricornutum, we present evidence that this pathway functions to divert excess plastidial glyceraldehyde-3-phosphate into diverse fates accessed from the pyruvate hub, and may potentially also function in the gluconeogenic direction to permit more efficient management of cellular carbon. Considering meta-genomic data, we show that this pathway is of greater importance in polar and sub-polar oceans, in which diatoms dominate primary production; and considering experimental data, we show that this principally relates to the elongated photoperiods present at high latitudes. Our data provide insights into the functions of a poorly understood yet evolutionarily recurrent plastidial metabolic pathway, and a further explanation for the success of diatoms in the contemporary ocean.

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Section: Resultsmentioning

confidence: 77%

Complementary environmental analysis and functional characterization of a plastid diatom lower glycolytic-gluconeogenesis pathway

Dorrell

Liang

Guéguen

et al. 2022

Preprint

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“…These approaches present differing strengths and weaknesses. MAGs are informative in terms of the functional gene repertoire of the community (Delmont et al, 2022), and can also be used for biodiversity assessment and taxonomic characterization (Frioux et al, 2020; Obiol et al, 2020; Karlusich et al, 2022), but the depth of these assessments can vary greatly, as the coverage is frequently insufficient to detect the taxa with low relative abundance (Ayling et al, 2019). Metabarcoding, in comparison, has a relatively limited capacity to predict the detailed functional diversity in the community, because the prediction depends on the availability of closely related reference sequences, and similarity in marker sequences does not guarantee similarity in genomic features (Pérez-Cobas A.E., 2020).…”

Section: Introductionmentioning

confidence: 99%

“…Metabarcoding, in comparison, has a relatively limited capacity to predict the detailed functional diversity in the community, because the prediction depends on the availability of closely related reference sequences, and similarity in marker sequences does not guarantee similarity in genomic features (Pérez-Cobas A.E., 2020). However, metabarcoding offers comparatively precise information in terms of taxonomic composition (Frioux et al, 2020; Grossart et al, 2020; Karlusich et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

On the relationship between protist metabarcoding and protist metagenome-assembled genomes

Zavadska,

Henry,

Auladell

et al. 2023

Preprint

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The two most commonly used approaches to study the composition of environmental protist communities are marker gene metabarcoding and whole genome analysis through metagenomics. Raw metabarcoding data are usually processed into Operational Taxonomic Units (OTUs) or amplicon sequence variants (ASVs) through clustering or denoising approaches, respectively. Analogous approaches have been developed to assemble metagenomic sequence reads into metagenome-assembled genomes (MAGs). Understanding the correspondence between the data produced by these two approaches can help to integrate information between the datasets and to explain how metabarcoding OTUs and MAGs are related with the underlying biological entities they are hypothesised to represent. Due to the nature of their construction, MAGs do not contain the most commonly used barcoding loci, meaning that sequence homology approaches cannot be used to match OTUs and MAGs.We made an attempt to match V9 metabarcoding OTUs from the 18S rRNA gene (V9 OTUs) and MAGs from theTaraOceans expedition (2009-2013) based on the correspondence of their relative abundances across the same set of samples. We evaluated the performance of several methods for detecting correspondence between features in these two compositional datasets and developed a series of controls to filter artefacts of data structure and processing. After selecting the best-performing correspondence metrics, ranking the V9 OTU/MAG matches by their proportionality/correlation coefficients and applying a set of selection criteria, we identified candidate matches between V9 OTUs and MAGs.In a subset of cases, V9 OTUs and MAGs could be successfully matched with one another with a one-to-one correspondence, implying that they likely represent the same underlying biological entity. More generally, matches we observed could be classified into 4 scenarios: Scenario I - one V9 OTU matches more than one MAG; Scenario II - more than one V9 OTU matches more than one MAG; Scenario III - more than one V9 OTU matches one MAG; Scenario IV - one V9 OTU matches one MAG.These diverse scenarios for V9 OTU-MAG matches illustrate the complex nature of the OTU/MAG relationship. Notably, we found some instances in which different OTU-MAG matches from the same taxonomic group were not classified in the same scenario, with all four scenarios possible even within the same taxonomic group, illustrating that factors beyond taxonomic lineage influence the relationship between OTUs and MAGs. Overall, each scenario produces a different interpretation of V9 OTUs, MAGs and how they compare in terms of the genomic and ecological diversity that they represent.

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New plastids, old proteins: repeated endosymbiotic acquisitions in kareniacean dinoflagellates

Novák Vanclová,

Nef,

Füssy

et al. 2024

EMBO Rep

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Dinoflagellates are a diverse group of ecologically significant micro-eukaryotes that can serve as a model system for plastid symbiogenesis due to their susceptibility to plastid loss and replacement via serial endosymbiosis. Kareniaceae harbor fucoxanthin-pigmented plastids instead of the ancestral peridinin-pigmented ones and support them with a diverse range of nucleus-encoded plastid-targeted proteins originating from the haptophyte endosymbiont, dinoflagellate host, and/or lateral gene transfers (LGT). Here, we present predicted plastid proteomes from seven distantly related kareniaceans in three genera (Karenia, Karlodinium, and Takayama) and analyze their evolutionary patterns using automated tree building and sorting. We project a relatively limited ( ~ 10%) haptophyte signal pointing towards a shared origin in the family Chrysochromulinaceae. Our data establish significant variations in the functional distributions of these signals, emphasizing the importance of micro-evolutionary processes in shaping the chimeric proteomes. Analysis of plastid genome sequences recontextualizes these results by a striking finding the extant kareniacean plastids are in fact not all of the same origin, as two of the studied species (Karlodinium armiger, Takayama helix) possess plastids from different haptophyte orders than the rest.

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Biogeographical Patterns and Genomes of Aquatic Photoautotrophs

Cited by 4 publications

References 160 publications

Complementary environmental analysis and functional characterization of a plastid diatom lower glycolytic-gluconeogenesis pathway

Complementary environmental analysis and functional characterization of a plastid diatom lower glycolytic-gluconeogenesis pathway

On the relationship between protist metabarcoding and protist metagenome-assembled genomes

New plastids, old proteins: repeated endosymbiotic acquisitions in kareniacean dinoflagellates

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