Ancient Recruitment by Chromists of Green Algal Genes Encoding Enzymes for Carotenoid Biosynthesis

Abstract

Chromist algae (stramenopiles, cryptophytes, and haptophytes) are major contributors to marine primary productivity. These eukaryotes acquired their plastid via secondary endosymbiosis, whereby an early-diverging red alga was engulfed by a protist and the plastid was retained and its associated nuclear-encoded genes were transferred to the host genome. Current data suggest, however, that chromists are paraphyletic; therefore, it remains unclear whether their plastids trace back to a single secondary endosymbiosis or, alternatively, this organelle has resulted from multiple independent events in the different chromist lineages. Both scenarios, however, predict that plastid-targeted, nucleus-encoded chromist proteins should be most closely related to their red algal homologs. Here we analyzed the biosynthetic pathway of carotenoids that are essential components of all photosynthetic eukaryotes and find a mosaic evolutionary origin of these enzymes in chromists. Surprisingly, about one-third (5/16) of the proteins are most closely related to green algal homologs with three branching within or sister to the early-diverging Prasinophyceae. This phylogenetic association is corroborated by shared diagnostic indels and the syntenic arrangement of a specific gene pair involved in the photoprotective xanthophyll cycle. The combined data suggest that the prasinophyte genes may have been acquired before the ancient split of stramenopiles, haptophytes, cryptophytes, and putatively also dinoflagellates. The latter point is supported by the observed monophyly of alveolates and stramenopiles in most molecular trees. One possible explanation for our results is that the green genes are remnants of a cryptic endosymbiosis that occurred early in chromalveolate evolution; that is, prior to the postulated split of stramenopiles, alveolates, haptophytes, and cryptophytes. The subsequent red algal capture would have led to the loss or replacement of most green genes via intracellular gene transfer from the new endosymbiont. We argue that the prasinophyte genes were retained because they enhance photosynthetic performance in chromalveolates, thus extending the niches available to these organisms. The alternate explanation of green gene origin via serial endosymbiotic or horizontal gene transfers is also plausible, but the latter would require the independent origins of the same five genes in some or all the different chromalveolate lineages.

High Light Acclimation in the Secondary Plastids Containing Diatom Phaeodactylum tricornutum is Triggered by the Redox State of the Plastoquinone Pool

“…All known enzymes involved in carotenoid synthesis are nucleus encoded, but the carotenoid synthesis itself takes place in the chloroplast (Coesel et al, 2008;Frommolt et al, 2008;Lohr, 2011). The Dd+Dt synthesis was unaffected by the nuclear translation inhibitor CHX; hence, its regulation must occur at the posttranslational stage and most probably in the chloroplast.…”

Distribution of the SELMA Translocon in Secondary Plastids of Red Algal Origin and Predicted Uncoupling of Ubiquitin-Dependent Translocation from Degradation

“…According to the chromalveolate hypothesis, six major lineages were grouped together to be of monophyletic origin: cryptophytes, haptophytes, heterokontophytes, peridinincontaining dinoflagellates, apicomplexans, and the non-plastidcontaining ciliates, as well as several smaller lineages related to some chromalveolate members (15, 41). However, recent phylogenetic analyses have given rise to extended theories about the evolution of the lineages with a red algal endosymbiont, including serial endosymbiotic events with secondary, as well as tertiary, endosymbioses (21,22,26,27,56,61,71,75).It has been shown that the lineages with an endosymbiont of red algal origin share common plastid protein import mechanisms despite remarkable differences resulting from specific features in plastid ultrastructure (10,37,65). Import into complex plastids starts cotranslationally at the endoplasmic reticulum (ER) membrane where nascent precursor proteins are synthesized into the ER lumen.…”

Analysis of horizontal genetic transfer in red algae in the post-genomics age

“…Recent studies that include the novel red algal genome data in the analysis do not show a significant reduction in the green gene footprint. 30,33,34 Furthermore, analysis of diatom genomes reveals green algal derived genes to encode functions relevant to plastid metabolism such as multiple components of the carotenoid biosynthesis pathway, 35 photoprotection under fluctuating light conditions, 36 membrane transport, 33 and fatty acid biosynthesis. 37 These might be the sorts of highly beneficial functions that would be maintained as remnants of a previous plastid of green algal provenance.…”