A host organelle integrates stolen chloroplasts for animal photosynthesis

  • Cell. 2025 Jun 21:S0092-8674(25)00637-3. doi: 10.1016/j.cell.2025.06.003.
Corey A H Allard  1 ,  Angus B Thies  2 ,  Rishav Mitra  3 ,  Patric M Vaelli  3 ,  Olivia D Leto  4 ,  Brittany L Walsh  3 ,  Elise M J Laetz  5 ,  Martin Tresguerres  2 ,  Amy S Y Lee  6 ,  Nicholas W Bellono  7
Affiliations
  • 1. Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA; Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA. Electronic address: [email protected].
  • 2. Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093, USA.
  • 3. Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
  • 4. Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA; Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA.
  • 5. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands.
  • 6. Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA; Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA 02115, USA. Electronic address: [email protected].
  • 7. Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA. Electronic address: [email protected].
PMID: 40570835 DOI: 10.1016/j.cell.2025.06.003
Abstract

Eukaryotic life evolved over a billion years ago when ancient cells engulfed and integrated prokaryotes to become modern mitochondria and chloroplasts. Sacoglossan "solar-powered" sea slugs possess the ability to acquire organelles within a single lifetime by selectively retaining consumed chloroplasts that remain photosynthetically active for nearly a year. The mechanism for this "animal photosynthesis" remains unknown. Here, we discovered that foreign chloroplasts are housed within novel, host-derived organelles we term "kleptosomes." Kleptosomes use ATP-sensitive ion channels to maintain a luminal environment that supports chloroplast photosynthesis and longevity. Upon slug starvation, kleptosomes digest stored chloroplasts for additional nutrients, thereby serving as a food source. We leveraged this discovery to find that organellar retention and digestion of photosynthetic cargo has convergently evolved in Other photosynthetic Animals, including corals and anemones. Thus, our study reveals mechanisms underlying the long-term acquisition and evolutionary incorporation of intracellular symbionts into organelles that support complex cellular function.

Keywords
cell biology; endosymbiosis; evolution; kleptoplasty; organellar ion channels; photosynthetic animal.
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