Synthesis of Several Light-Harvesting Complex I Polypeptides Is Blocked by Cycloheximide in Symbiotic Chloroplasts in the Sea Slug,Elysia chlorotica(Gould): A Case for Horizontal Gene Transfer Between Alga and Animal?

Abstract

The chloroplast symbiosis between the ascoglossan (=Sacoglossa) sea slug Elysia chlorotica and plastids from the chromophytic alga Vaucheria litorea is the longest-lived relationship of its kind known, lasting up to 9 months. During this time, the plastids continue to photosynthesize in the absence of the algal nucleus at rates sufficient to meet the nutritional needs of the slugs. We have previously demonstrated that the synthesis of photosynthetic proteins occurs while the plastids reside within the diverticular cells of the slug. Here, we have identified several of these synthesized proteins as belonging to the nuclear-encoded family of polypeptides known as light-harvesting complex I (LHCI). The synthesis of LHCI is blocked by the cytosolic ribosomal inhibitor cycloheximide and proceeds in the presence of chloramphenicol, a plastid ribosome inhibitor, indicating that the gene encoding LHCI resides in the nuclear DNA of the slug. These results suggest that a horizontal transfer of the LHCI gene from the alga to the slug has taken place.

Sea Slug Kleptoplasty and Plastid Maintenance in a Metazoan

“…Until recently, these studies used the candidate gene approach to putatively identify alga-derived genes in the animal. The methods have included PCR (Green et 2009; Rumpho et al, 2008Rumpho et al, , 2009), detection of de novo synthesis of nucleus-encoded plastid proteins using radiolabeling and immunolabeling in combination with specific inhibitors of transcription or translation (Pierce et al, , 2007Green et al, 2000;Hanten and Pierce, 2001;Rumpho et al, 2001Rumpho et al, , 2009, northern-blot analysis and genome walking (Rumpho et al, 2008), 14 C incorporation and synthesis of chlorophyll in animal tissue (Pierce et al, 2009), and quantitative reverse transcription-PCR of nucleus-encoded algal genes in the animal ). All of these data support the presence of a few (Rumpho et al, 2008(Rumpho et al, , 2009) to numerous (Pierce et al, 2009;Schwartz et al, 2010) nuclear algal genes or gene fragments in E. chlorotica.…”

Branched Mitochondrial Electron Transport in the Animalia: Presence of Alternative Oxidase in Several Animal Phyla

“…For example, a cellulose synthase gene in C. intestinalis and the possible presence of algal photosynthetic genes in a molluscan sea slug are suggested to represent horizontal gene transfer events (40,41). Despite such examples, it seems unlikely that animals from three different phyla would be subject to horizontal gene transfer events resulting in animal AOX genes so similar to one another (Fig.…”

Chlorophyll a synthesis by an animal using transferred algal nuclear genes

“…Certain cells that line the slug's digestive diverticula are able to phagocytize undigested chloroplasts which are maintained intracellularly, and continue to be photosynthetically active for as long as the 10-11 month life cycle of the slug (West et al, 1984). Although there is no evidence of chloroplast division in the slug cytoplasm, synthesis of several chloroplast proteins occurs during the endosymbiotic association, including proteins that are encoded by algal nuclear genes (Pierce et al, 1996;Hanten and Pierce, 2001). Our original discovery found expressed genes for three of the algal light-harvesting complex proteins, LHCV-1, LHCV-2 and FCP, in genomic DNA of the slug (Pierce et al, 2007).…”