Acquired Phototrophy in Ciliates: A Review of Cellular Interactions and Structural Adaptations1

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.

Plastid-bearing sea slugs fix CO2in the light but do not require photosynthesis to survive

“…Symbioses between animals or heterotrophic protist and algae are fairly common in nature [1]; prominent examples include the zoochlorellae of Hydra viridis [2,3] or dinoflagellates (zooxanthellae) of corals [4] and the many different species of algae found in ciliates [5]. A more curious kind of symbiosis is found among the sacoglossan molluscs (marine slugs) from the Plakobranchoidea.…”

The Importance of Mesodinium rubrum at Post-Spring Bloom Nutrient and Phytoplankton Dynamics in the Vertically Stratified Baltic Sea

“…rubrum is extremely mobile, known to be fastest autotroph in the sea with a swimming velocity that is reported to reach 8.5 mm s −1 (30 m h −1 ; Smayda, 2010) and showing marked phototaxis and vertical migrations (Lindholm, 1985). Some studies already a long time ago demonstrated the very high rate of primary production of this species (e.g., Mackenzie and Gillespie, 1986;Crawford, 1989;Stoecker et al, 1991; review by Johnson, 2011). Increased temperature and water column stability, decreased salinity and depletion of dissolved inorganic nitrogen from the surface layer are known to have positive influence to the occurrence and abundance of M. rubrum (Lindholm and Mörk, 1990;Cloern et al, 1994;Montagnes et al, 2008;Johnson et al, 2013) in different locations worldwide.…”

Seasonal and Interannual Changes in Ciliate and Dinoflagellate Species Assemblages in the Arctic Ocean (Amundsen Gulf, Beaufort Sea, Canada)

“…Microzooplankton species, especially dinoflagellates, use a variety of techniques to capture prey (e.g., Nielsen and Kiørboe, 2015), with some ciliates being fastidious in terms of nutritional requirements (e.g., Johnson, 2011), and others having a narrow size specificity range (e.g., Park and Kim, 2010). Because of such selectivity, microzooplankton could have a top-down effect on phytoplankton and protist community composition (Irigoien, 2005), with implications for microbial food webs, nutrient, and carbon cycles, as well as zooplankton nutrition and higher food webs.…”