A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids

Abstract

BackgroundLight, the driving force of photosynthesis, can be harmful when present in excess; therefore, any light harvesting system requires photoprotection. Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages.ResultsHere, we demonstrate that the recently discovered “red lineage chlorophyll a/b-binding-like proteins” (RedCAPs) form a monophyletic family within this protein superfamily. The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin). Expression of a full-length RedCAP:GFP fusion construct in the diatom Phaeodactylum tricornutum confirmed the predicted plastid localisation of RedCAPs. Furthermore, we observed that similarly to the fucoxanthin chlorophyll a/c-binding light-harvesting antenna proteins also RedCAP transcripts in diatoms were regulated in a diurnal way at standard light conditions and strongly repressed at high light intensities.ConclusionsThe absence of RedCAPs from the green lineage implies that RedCAPs evolved in the red lineage after separation from the the green lineage. During the evolution of secondary plastids, RedCAP genes therefore must have been transferred from the nucleus of the endocytobiotic alga to the nucleus of the host cell, a process that involved complementation with pre-sequences allowing import of the gene product into the secondary plastid bound by four membranes. Based on light-dependent transcription and on localisation data, we propose that RedCAPs might participate in the light (intensity and quality)-dependent structural or functional reorganisation of the light-harvesting antennae of the photosystems upon dark to light shifts as regularly experienced by diatoms in nature. Remarkably, in plastids of the red lineage as well as in green lineage plastids, the phycobilisome based cyanobacterial light harvesting system has been replaced by light harvesting systems that are based on members of the extended LHC protein superfamily, either for one of the photosystems (PS I of red algae) or for both (diatoms). In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.

Allosteric communication between DNA-binding and light-responsive domains of diatom class I aureochromes

“…The expression patterns of four aureochrome paralogs in P. tricornutum were investigated to screen for their light-dependent differential expression using cDNA generated earlier ( 25 ). In short, cells had been pre-adapted to 16 h of daily illumination with low light (LL) and had been either kept under the same condition or transferred to continuous darkness for one illumination period.…”

Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage

“…Experimental data were compiled from published studies (Liaud et al, 2000;Apt et al, 2002;Domergue et al, 2003;Kroth, 2004, 2005;Kroth et al, 2005;Tanaka et al, 2005;Gould et al, 2006b;Gruber et al, 2007Gruber et al, , 2009Lepetit et al, 2007;Siaut et al, 2007;Sommer et al, 2007;Kitao et al, 2008;Ast et al, 2009;Hempel et al, 2009Hempel et al, , 2010Kitao and Matsuda, 2009;Weber et al, 2009;Bullmann et al, 2010;Felsner et al, 2010;Joshi-Deo et al, 2010;Allen et al, 2011Allen et al, , 2012Bruckner et al, 2011;Grouneva et al, 2011;Moog et al, 2011;Tachibana et al, 2011;Vugrinec et al, 2011;Sturm et al, 2013). The gene models for the experi-mentally tested proteins were manually verified (Table S3).…”

Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

“…Porphyra has the same complement of genes (SI Appendix, Table S19) to carry out photosynthesis as other red algae, but exhibits a notable set of photoprotection strategies. Among the 13 genes encoding chlorophyll a-binding light-harvesting complex proteins are two "RedCap" genes (42), which may be involved in reorganization of the photosynthetic antenna during the shift from darkness to light (43). Porphyra also has 11 genes encoding "high light-induced" or "one-helix" proteins (here OHPs) that have essential roles for photoacclimation and cell viability under stressful environmental conditions (43,44).…”

“…Among the 13 genes encoding chlorophyll a-binding light-harvesting complex proteins are two "RedCap" genes (42), which may be involved in reorganization of the photosynthetic antenna during the shift from darkness to light (43). Porphyra also has 11 genes encoding "high light-induced" or "one-helix" proteins (here OHPs) that have essential roles for photoacclimation and cell viability under stressful environmental conditions (43,44). Mechanistically, OHPs may regulate chlorophyll and tetrapyrrole biosynthesis, stabilize photosystem I (PSI), bind free chlorophyll or chlorophyllbreakdown products from damaged PSII complexes during the damage/repair cycle, or bind carotenoids that dissipate excess absorbed light energy.…”