Abstract
The light-harvesting complex (LHC) is an essential component in light energy capture and transduction to facilitate downstream photosynthetic reactions in plant and algal chloroplasts. The unicellular dinoflagellate alga Symbiodinium is an endosymbiont of cnidarian animals, including corals and sea anemones, and provides carbohydrates generated through photosynthesis to host animals. Although Symbiodinium possesses a unique LHC gene family, called chlorophyll a-chlorophyll c2-peridinin protein complex (acpPC), its genome-level diversity and evolutionary trajectories have not been investigated. Here, we describe a phylogenetic analysis revealing that many of the LHCs are encoded by highly duplicated genes with multi-subunit polyprotein structures in the nuclear genome of Symbiodinium minutum. This analysis provides an extended list of the LHC gene family in a single organism, including 80 loci encoding polyproteins composed of 145 LHC subunits recovered in the phylogenetic tree. In S. minutum, 5 phylogenetic groups of the Lhcf-type gene family, which is exclusively conserved in algae harboring secondary plastids of red algal origin, were identified. Moreover, 5 groups of the Lhcr-type gene family, of which members are known to be associated with PSI in red algal plastids and secondary plastids of red algal origin, were identified. Notably, members classified within a phylogenetic group of the Lhcf-type (group F1) are highly duplicated, which may explain the presence of an unusually large number of LHC genes in this species. Some gene units were homologous to other units within single loci of the polyprotein genes, whereas intergenic homologies between separate loci were conspicuous in other cases, implying that gene unit ‘shuffling’ by gene conversion and/or genome rearrangement might have been a driving force for diversification. These results suggest that vigorous intra- and intergenic gene duplication events have resulted in the genomic framework of photosynthesis in coral symbiont dinoflagellate algae.
Highlights
Light harvesting complex (LHC) proteins are peripheral components of photosystem (PS) I and PSII and essential for receiving and transferring light energy to the core machinery of the photosystems as well as dissipating such energy as heat under excess light conditions [1,2]
The function and composition of the photosystems, including their LHCs, have been extensively studied using the model land plant Arabidopsis thaliana and the model green alga Chlamydomonas reinhardtii, far fewer studies have investigated LHCs in other lineages, e.g., chlorophyll a-binding LHCs encoded by Lhcr genes in ‘red lineage’ organisms including red algae and algae harboring secondary plastids of red algal origin, fucoxanthin chlorophyll a/c-binding LHCs (FCP) encoded by Lhcf genes in stramenopiles, and chlorophyll a-chlorophyll c2-peridinin protein complex in dinoflagellates [3,4]
We removed redundant polypeptide sequences derived from alternatively spliced RNAseq contigs and generated a dataset composed of 164 LHC proteins, with each encompassing three trans-membrane helices, out of 82 loci of genes encoding polyproteins
Summary
Light harvesting complex (LHC) proteins are peripheral components of photosystem (PS) I and PSII and essential for receiving and transferring light energy to the core machinery of the photosystems as well as dissipating such energy as heat under excess light conditions [1,2]. Phylogenetic analysis showed that S. minutum possessed genes encoding three groups of LHC family proteins: LHCR-type, LHCF-type and a group composed of two miscellaneous LHC-like proteins encoded by a single gene locus (ID 028830)
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