Evolutionary transition towards permanent chloroplasts? - Division of kleptochloroplasts in starved cells of two species of Dinophysis (Dinophyceae)

PLoS One. 2017 May 11;12(5):e0177512. doi: 10.1371/journal.pone.0177512. eCollection 2017.

Abstract

Species within the marine toxic dinoflagellate genus Dinophysis are phagotrophic organisms that exploit chloroplasts (kleptochloroplasts) from other protists to perform photosynthesis. Dinophysis spp. acquire the kleptochloroplasts from the ciliate Mesodinium rubrum, which in turn acquires the chloroplasts from a unique clade of cryptophytes. Dinophysis spp. digest the prey nuclei and all other cell organelles upon ingestion (except the kleptochloroplasts) and they are therefore believed to constantly acquire new chloroplasts as the populations grow. Previous studies have, however, indicated that Dinophysis can keep the kleptochloroplasts active during long term starvation and are able to produce photosynthetic pigments when exposed to prey starvation. This indicates a considerable control over the kleptochloroplasts and the ability of Dinophysis to replicate its kleptochloroplasts was therefore re-investigated in detail in this study. The kleptochloroplasts of Dinophysis acuta and Dinophysis acuminata were analyzed using confocal microscopy and 3D bioimaging software during long term starvation experiments. The cell concentrations were monitored to confirm cell divisions and samples were withdrawn each time a doubling had occurred. The results show direct evidence of kleptochloroplastidic division and that the decreases in total kleptochloroplast volume, number of kleptochloroplasts and number of kleptochloroplast centers were not caused by dilution due to cell divisions. This is the first report of division of kleptochloroplasts in any protist without the associated prey nuclei. This indicates that Dinophysis spp. may be in a transitional phase towards possessing permanent chloroplasts, which thereby potentially makes it a key organism to understand the evolution of phototrophic protists.

MeSH terms

  • Biological Evolution*
  • Cell Division
  • Chloroplasts / genetics*
  • Dinoflagellida / cytology
  • Dinoflagellida / genetics*
  • Dinoflagellida / radiation effects
  • Light
  • Microscopy, Fluorescence

Grants and funding

This study was partly supported by the Danish Council for Independent Research, grant number 4181-00484 to PJH. ND thanks the Villum Kann Rasmussen Foundation for an equipment grant.