Prey type constrains growth and photosynthetic capacity of the kleptoplastidic ciliate Mesodinium chamaeleon (Ciliophora).

Kleptoplastidic, or chloroplast-stealing, lineages offer insight into the process of acquiring photosynthesis. By quantifying the ability of these organisms to retain and use photosynthetic machinery from their prey, we can understand how intermediaries on the endosymbiosis pathway might have evolved regulatory and maintenance mechanisms. Here, we focus on a mixotrophic kleptoplastidic ciliate, Mesodinium chamaeleon, noteworthy for its ability to retain functional chloroplasts from at least half a dozen cryptophyte algal genera. We contrasted the performance of kleptoplastids from blue-green and red cryptophyte prey as a function of light level and feeding history. Our experiments showed that starved M. chamaeleon cells are able to maintain photosynthetic function for at least 2 weeks and that M. chamaeleon containing red plastids lost chlorophyll and electron transport capacity faster than those containing blue-green plastids. However, likely due to increased pigment content and photosynthetic rates in red plastids, M. chamaeleon had higher growth rates and more prolonged growth when feeding on red cryptophytes. For example, M. chamaeleon grew rapidly and extensively when fed the blue-green cryptophyte Chroomonas mesostigmatica, but this growth appeared to hinge on high levels of feeding supporting photosynthetic activity. In contrast, even starved M. chamaeleon containing red plastids from Rhodomonas salina could achieve high photosynthetic rates and extensive growth. Our findings show that plastid origin impacts the maintenance and magnitude of photosynthetic activity, though whether this is due to variation in ciliate control or gradual loss of plastid function in ingested prey cells remains unknown.

Intra-host Symbiont Diversity and Extended Symbiont Maintenance in Photosymbiotic Acantharea (Clade F).

Photosymbiotic protists contribute to surface primary production in low-nutrient, open-ocean ecosystems and constitute model systems for studying plastid acquisition via endosymbiosis. Little is known, however, about host-symbiont dynamics in these important relationships, and whether these symbioses are mutualistic is debated. In this study, we applied single-cell sequencing methods and advanced fluorescent microscopy to investigate host-symbiont dynamics in clade F acantharians, a major group of photosymbiotic protists in oligotrophic subtropical gyres. We amplified the 18S rRNA gene from single acantharian hosts and environmental samples to assess intra-host symbiont diversity and to determine whether intra-host symbiont community composition directly reflects the available symbiont community in the surrounding environment. Our results demonstrate that clade F acantharians simultaneously host multiple species from the haptophyte genera Phaeocystis and Chrysochromulina. The intra-host symbiont community composition was distinct from the external free-living symbiont community, suggesting that these acantharians maintain symbionts for extended periods of time. After selectively staining digestive organelles, fluorescent confocal microscopy showed that symbionts were not being systematically digested, which is consistent with extended symbiont maintenance within hosts. Extended maintenance within hosts may benefit symbionts through protection from grazing or viral lysis, and therefore could enhance dispersal, provided that symbionts retain reproductive capacity. The evidence for extended symbiont maintenance therefore allows that Phaeocystis could glean some advantage from the symbiosis and leaves the possibility of mutualism.