: 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.
The availability of CO2 is one of the restrictions on aquatic photosynthesis. Solute carrier (SLC) 4-2, a plasma membrane HCO3- transporter, was previously identified in the marine diatom, Phaeodactylum tricornutum. In this study, we discovered two paralogs, PtSLC4-1 and PtSLC4-4, and localized both at the plasma membrane. Their overexpression stimulated HCO3- uptake, which were inhibited by 4,4'-diisothiocyanostilbene-2,2’-disulfonic (DIDS), an anion channel blocker. Furthermore, PtSLC4-1, similarly to SLC4-2, required specifically Na + of about 100 mM for its maximum HCO3- transport activity. Unlike PtSLC4-1 and PtSLC4-2, the HCO3- transport of PtSLC4-4 depends equally on Na +, K +, or Li +, suggesting its broad selectivity for cations. Transcript analyses indicate that PtSLC4-1 is the most abundant HCO3- transporter under CO2 below atmospheric level, while PtSLC4-4 showed little transcript induction in atmospheric CO2 but temporal induction to the comparable levels to PtSLC4-1 at an initial acclimation stage from high CO2 (1%) to very low CO2 (<0.002%). The data strongly suggest the major HCO3- transport role of PtSLC4-1 with relatively minor role of PtSLC4-2, and that PtSLC4-4 operates under severe CO2 limitation when other SLC4s do not function to support an urgent HCO3- uptake unselectively to cations.
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