Abstract
Of all the eukaryotic algal groups, diatoms make the most substantial contributions to photosynthesis in the contemporary ocean. Understanding the biological innovations that have occurred in the diatom chloroplast may provide us with explanations to the ecological success of this lineage and clues as to how best to exploit the biology of these organisms for biotechnology. In this paper, we use multi-species transcriptome datasets to compare chloroplast metabolism pathways in diatoms to other algal lineages. We identify possible diatom-specific innovations in chloroplast metabolism, including the completion of tocopherol synthesis via a chloroplast-targeted tocopherol cyclase, a complete chloroplast ornithine cycle, and chloroplast-targeted proteins involved in iron acquisition and CO2 concentration not shared between diatoms and their closest relatives in the stramenopiles. We additionally present a detailed investigation of the chloroplast metabolism of the oil-producing diatom Fistulifera solaris, which is of industrial interest for biofuel production. These include modified amino acid and pyruvate hub metabolism that might enhance acetyl-coA production for chloroplast lipid biosynthesis and the presence of a chloroplast-localised squalene synthesis pathway unknown in other diatoms. Our data provides valuable insights into the biological adaptations underpinning an ecologically critical lineage, and how chloroplast metabolism can change even at a species level in extant algae.
Highlights
Institut de Biologie de l’ENS (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France
The diatom chloroplast performs effectively all of the essential pathways identified in plant chloroplasts, including photosynthesis, central carbon and lipid metabolism, synthesis of plastidial amino acids, chlorophyll and carotenoid synthesis, and essential plastid biogenesis pathways associated with expression of the chloroplast genome and protein import [25,58,61] (Figure 3A)
In contrast to the situation for theta-carbonic anhydrases, there was no apparent bias in favour of chloroplast-targeted proteins in diatoms compared to other stramenopile, haptophyte or cryptomonad groups, with a greater proportion of pelagophyte and dictyochophyte sequences possessing chloroplast-targeting peptides (Figure 5A; Table S2), suggesting it is an evolutionary innovation that precedes the origins of the diatom chloroplast
Summary
Against the backdrop of rising atmospheric carbon dioxide concentrations and anthropogenic climate change, it is increasingly important to understand how photosynthesis functions in the ocean [1]. Diatoms dominate in polar waters and provinces that are chronically low in iron [3] and are the main photosynthetic producers in waters classified as ‘high in nutrients, low in chlorophyll’ (HNLC), notably large swathes of the Southern Ocean, equatorial Pacific Ocean, and north Pacific Ocean They are not obligately oligotrophic species and bloom seasonally when nutrient or physical conditions change. Ocean acidification may adversely affect nutrient acquisition and photoprotection in diatoms, this remains debated [9] Alongside their environmental abundance, the diatom group includes various phenotypes with possible agricultural and industrial applications, many of which may be lineage- or even species-specific. We explore specific biochemical adaptations associated with the chloroplasts of one diatom species, the biofuel producer F. solaris
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