The genome of a nonphotosynthetic diatom provides insights into the metabolic shift to heterotrophy and constraints on the loss of photosynthesis

Pendergrass, Anastasiia; Roberts, Wade R.; Ruck, Elizabeth C.; Lewis, Jeffrey A.; Alverson, Andrew J.

doi:10.1101/2020.05.28.115543

Cited by 4 publications

(4 citation statements)

References 124 publications

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“…(Nitz4; Fig. S6) (46). Both Random Forest and XGBoost successfully classified this diatom as heterotrophic despite the presence of four photosynthetic Nitzschia species within the training set, reiterating the ability of the model to disentangle phylogeny and trophic status.…”

Section: Resultsmentioning

confidence: 99%

The dynamic trophic architecture of open-ocean protist communities revealed through machine-guided metatranscriptomics

Lambert

Groussman

Schatz

et al. 2021

Preprint

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Intricate networks of single-celled eukaryotes (protists) dominate carbon flow in the ocean. Their growth, demise, and interactions with other microorganisms drive the fluxes of biogeochemical elements through marine ecosystems. Mixotrophic protists are capable of both photosynthesis and ingestion of prey and are dominant components of open-ocean planktonic communities. Yet, the role of mixotrophs in elemental cycling is obscured by their capacity to act as primary producers or heterotrophic consumers depending on factors that remain largely uncharacterized. Here we introduce a machine learning model that can predict the in situ nutritional mode of aquatic protists based on their patterns of gene expression. This approach leverages a public collection of protist transcriptomes as a training set to identify a subset of gene families whose transcriptional profiles predict trophic status. We applied our model to nearly 100 metatranscriptomes obtained during two oceanographic cruises in the North Pacific and found community-level and population-specific evidence that abundant open-ocean mixotrophic populations shift their predominant mode of nutrient and carbon acquisition in response to natural gradients in nutrient supply and sea surface temperature. In addition, metatranscriptomic data from ship-board incubation experiments revealed that abundant mixotrophic prymnesiophytes from the oligotrophic North Pacific subtropical gyre rapidly remodelled their transcriptome to enhance photosynthesis when supplied with limiting nutrients. Coupling the technique introduced here with experiments designed to reveal the mechanisms driving mixotroph physiology is a promising approach for understanding the ecology of mixotrophic populations in the natural environment.Significance statementMixotrophy is a ubiquitous nutritional strategy in marine ecosystems. Although our understanding of the distribution and abundance of mixotrophic plankton has improved significantly, the functional roles of mixotrophs are difficult to pinpoint, as mixotroph nutritional strategies are flexible and form a continuum between heterotrophy and phototrophy. We employ a machine learning-driven metatranscriptomic technique to assess the nutritional strategies of abundant planktonic populations in situ and demonstrate that mixotrophic populations play varying functional roles along physico-chemical gradients in the North Pacific Ocean, revealing a degree of physiological plasticity unique to aquatic mixotrophs. Our results highlight mechanisms that may dictate the flow of biogeochemical elements and the ecology of the North Pacific Ocean, one of the largest biogeographical provinces on Earth.

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Section: Resultsmentioning

confidence: 99%

The dynamic trophic architecture of open-ocean protist communities revealed through machine-guided metatranscriptomics

Lambert

Groussman

Schatz

et al. 2021

Preprint

Self Cite

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“…1). These include some lineages that resolve within otherwise photosynthetic groups, e.g., non-photosynthetic diatoms (26,27), dictyochophytes (28,29), and chrysophytes (23,30), and accordingly retain leucoplasts (non-photosynthetic plastids). Other non-photosynthetic stramenopile groups contain no photosynthetic members and no trace of plastids.…”

Section: Haptophytes Chlorarachniophytes Euglenids Dinoflagellatesmentioning

confidence: 99%

“…Ultimately, further functional characterisation is required to understand the metabolic contributions of the Nitzschia leucoplast in the context of other, secondarily non-photosynthetic algal species. ; which will be aided by the recent completion of a nuclear transcriptome (120) and draft genome (27).…”

Section: Diatom Leucoplast Genomesmentioning

confidence: 99%

Reconstructing Dynamic Evolutionary Events in Diatom Nuclear and Organelle Genomes

Dorrell

Liu

Bowler

2022

The Molecular Life of Diatoms

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The diatoms evolved within the stramenopiles, an ecologically important and diverse assemblage of eukaryotes that includes both photosynthetic macrophytes and microalgae, as well as non-photosynthetic heterotrophs and parasites. The evolutionary history of the stramenopiles, which stretches back to the Palaeozoic, has been marked by the acquisition of chloroplasts in a recent common ancestor of their photosynthetic members, the ochrophytes; and progressive gains of genes in the nuclear genome by horizontal and endosymbiotic gene transfer. Here, we place diatoms in their actual evolutionary context within the stramenopiles; identify gene transfers that have shaped the coding content of the diatom nucleus; and profile sources of differences in chloroplast and mitochondrial genome content between different stramenopiles including diatoms. We underline the importance of considering diatoms as evolutionary mosaics, supported by genes of bacterial, red, green and other eukaryotic algal origin as illustrated by multiple phylogenomic studies realised over the last two decades; and the relatively limited changes to organelle genome content in diatoms compared to other stramenopile lineages. However, we identify a previously undocumented transfer of a novel open reading frame of the chloroplasts of green algae into the ochrophytes, underlining the importance of changes in organelle and nuclear gene content, in defining the current biology of diatoms.

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“…radians), oceanic (Thalassiosira oceanica), biofilm-forming (Seminavis robusta), and heterotrophic (Nitzschia sp.) species [4][5][6][7][8][9]. Apart from their ecological role, diatoms are also suitable for several biotechnological applications.…”

Section: Introductionmentioning

confidence: 99%

Mini-Review: Potential of Diatom-Derived Silica for Biomedical Applications

et al. 2021

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Diatoms are unicellular eukaryotic microalgae widely distributed in aquatic environments, possessing a porous silica cell wall known as frustule. Diatom frustules are considered as a sustainable source for several industrial applications because of their high biocompatibility and the easiness of surface functionalisation, which make frustules suitable for regenerative medicine and as drug carriers. Frustules are made of hydrated silica, and can be extracted and purified both from living and fossil diatoms using acid treatments or high temperatures. Biosilica frustules have proved to be suitable for biomedical applications, but, unfortunately, they are not officially recognised as safe by governmental food and medical agencies yet. In the present review, we highlight the frustule formation process, the most common purification techniques, as well as advantages and bottlenecks related to the employment of diatom-derived silica for medical purposes, suggesting possible solutions for a large-scale biosilica production.

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The genome of a nonphotosynthetic diatom provides insights into the metabolic shift to heterotrophy and constraints on the loss of photosynthesis

Cited by 4 publications

References 124 publications

The dynamic trophic architecture of open-ocean protist communities revealed through machine-guided metatranscriptomics

The dynamic trophic architecture of open-ocean protist communities revealed through machine-guided metatranscriptomics

Reconstructing Dynamic Evolutionary Events in Diatom Nuclear and Organelle Genomes

Mini-Review: Potential of Diatom-Derived Silica for Biomedical Applications

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