Acquired Phototrophy in Ciliates: A Review of Cellular Interactions and Structural Adaptations^†

ABSTRACT. Many ciliates acquire the capacity for photosynthesis through stealing plastids or harboring intact endosymbiotic algae. Both phenomena are a form of mixotrophy and are widespread among ciliates. Mixotrophic ciliates may be abundant in freshwater and marine ecosystems, sometimes making substantial contributions toward community primary productivity. While mixotrophic ciliates utilize phagotrophy to capture algal cells, their endomembrane system has evolved to partially bypass typical heterotrophic digestion pathways, enabling metabolic interaction with foreign cells or organelles. Unique adaptations may also be found in certain algal endosymbionts, facilitating establishment of symbiosis and nutritional interactions, while reducing their fitness for survival as free-living cells. Plastid retaining oligotrich ciliates possess little selectivity from which algae they sequester plastids, resulting in unstable kleptoplastids that require frequent ingestion of algal cells to replace them. Mesodinium rubrum (=Myrionecta rubra) possesses cryptophyte organelles that resemble a reduced endosymbont, and is the only ciliate capable of functional phototrophy and plastid division. Certain strains of M. rubrum may have a stable association with their cryptophyte organelles, while others need to acquire a cryptophyte nucleus through feeding. This process of stealing a nucleus, termed karyoklepty, was first described in M. rubrum and may be an evolutionary precursor to a stable, reduced endosymbiont, and perhaps eventually a tertiary plastid. The newly described Mesodinium“chamaeleon,” however, is less selective of which cryptophyte species it will retain organelles, and appears less capable of sustained phototrophy. Ciliates likely stem from a phototrophic ancestry, which may explain their propensity to practice acquired phototrophy.