Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

Mary E. Rumpho, Jared M. Worful, Jungho Lee, Krishna Kannan, Mary S. Tyler, Debashish Bhattacharya, Ahmed Moustafa, James R. Manhart

Research output: Contribution to journalArticlepeer-review

171 Scopus citations

Abstract

The sea slug Elysia chlorotica acquires plastids by ingestion of its algal food source Vaucheria litorea. Organelles are sequestered in the mollusc's digestive epithelium, where they photosynthesize for months in the absence of algal nucleocytoplasm. This is perplexing because plastid metabolism depends on the nuclear genome for >90% of the needed proteins. Two possible explanations for the persistence of photosynthesis in the sea slug are (i) the ability of V. litorea plastids to retain genetic autonomy and/or (ii) more likely, the mollusc provides the essential plastid proteins. Under the latter scenario, genes supporting photosynthesis have been acquired by the animal via horizontal gene transfer and the encoded proteins are retargeted to the plastid. We sequenced the plastid genome and confirmed that it lacks the full complement of genes required for photosynthesis. In support of the second scenario, we demonstrated that a nuclear gene of oxygenic photosynthesis, psbO, is expressed in the sea slug and has integrated into the germline. The source of psbO in the sea slug is V. litorea because this sequence is identical from the predator and prey genomes. Evidence that the transferred gene has integrated into sea slug nuclear DNA comes from the finding of a highly diverged psbO 3′ flanking sequence in the algal and mollusc nuclear homologues and gene absence from the mitochondrial genome of E. chlorotica. We demonstrate that foreign organelle retention generates metabolic novelty ("green animals") and is explained by anastomosis of distinct branches of the tree of life driven by predation and horizontal gene transfer.

Original languageEnglish (US)
Pages (from-to)17867-17871
Number of pages5
JournalProceedings of the National Academy of Sciences of the United States of America
Volume105
Issue number46
DOIs
StatePublished - Nov 18 2008
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • General

Keywords

  • Evolution
  • Plastid
  • Stramenopile
  • Symbiosis
  • Vaucheria litorea

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