A Phylogenetic Assessment of the Eukaryotic Light-Harvesting Antenna Proteins, with Implications for Plastid Evolution

Abstract

The light-harvesting complexes (LHCs) are a superfamily of chlorophyll-binding proteins present in all photosynthetic eukaryotes. The Lhc genes are nuclear-encoded, yet the pigment-protein complexes are localized to the thylakoid membrane and provide a marker to follow the evolutionary paths of plastids with different pigmentation. The LHCs are divided into the chlorophyll a/b-binding proteins of the green algae, euglenoids, and higher plants and the chlorophyll a/c-binding proteins of various algal taxa. This work examines the phylogenetic position of the LHCs from three additional taxa: the rhodophytes, the cryptophytes, and the chlorarachniophytes. Phylogenetic analysis of the LHC sequences provides strong statistical support for the clustering of the rhodophyte and cryptomonad LHC sequences within the chlorophyll a/c-binding protein lineage, which includes the fucoxanthin-chlorophyll proteins (FCP) of the heterokonts and the intrinsic peridinin-chlorophyll proteins (iPCP) of the dinoflagellates. These associations suggest that plastids from the heterokonts, haptophytes, cryptomonads, and the dinoflagellate, Amphidinium, evolved from a red algal-like ancestor. The Chlorarachnion LHC is part of the chlorophyll a/b-binding protein assemblage, consistent with pigmentation, providing further evidence that its plastid evolved from a green algal secondary endosymbiosis. The Chlorarachnion LHC sequences cluster with the green algal LHCs that are predominantly associated with photosystem II (LHCII). This suggests that the green algal endosymbiont that evolved into the Chlorarachnion plastid was acquired following the emergence of distinct LHCI and LHCII complexes.

Was “molecular opportunism” a factor in the evolution of different photosynthetic light-harvesting pigment systems?

“…Sequencing showed that they were indeed members of the LHC superfamily, even though they bound only Chl a and were associated only with photosystem I (6 -8). This showed that phycobilisomes (associated primarily with PSII) and membrane-intrinsic antennas of the LHC superfamily could coexist in the same chloroplast, and strongly supported a common evolutionary origin for all chloroplasts (8). In addition, it suggested that ancestral members of the LHC family may have had a considerable degree of f lexibility in pigment binding, so they were able to adapt to binding a variety of different Chls and carotenoids.…”

“…These features might be expected to impede the binding of Chl c to a Chl a site and even diminish protein folding, but this was not found in the experiments of Grabowski et al (9). All of these experiments suggest that the differences in sequence among the LHC proteins (8) optimizing energy transfer, binding carotenoids, and forming protein-protein interactions than with binding a specific Chl.…”

Chlorophyll and carotenoid binding in a simple red algal light-harvesting complex crosses phylogenetic lines

“…Heinemann and Paulsen (38) showed that a point mutation in such a domain of LHCII abolished in vitro reconstitution, suggesting that it is critical for assembly of a functional complex possibly because carotenoid binding cannot occur. However, conservation of the putative carotenoid binding sites is not consistent across taxa (11,39). In any case, it is difficult to imagine how these putative carotenoid binding sites could accommodate eight or more carotenoid molecules in one LHC polypeptide.…”

“…The LHCs of the red alga P. cruentum (LhcaR1, LhcaR2) are similar in sequence and predicted structure to LHCs of green plants and of other algae (6, 10), but phylogenetic analyses suggest a closer phylogenetic affinity with LHCs of chromophytes and dinophytes than with those of chlorophytes (11). Three transmembrane helices are a common feature of most LHCs, with eight conserved Chl-binding sites in chromophytes, dinophytes, and rhodophytes (6,10,12).…”

“…Analysis of primary amino acid sequences has been used to predict phylogenetic relatedness of LHCs (11). However, testing the relatedness, i.e., ascertaining the binding of heterologous pigments to individual LHC proteins, is presently beyond in vivo molecular genetic approaches.…”