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

Abstract

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.

Keywords: Mesodiniidae; acquired phototrophy; cryptophyte algae; kleptoplasty; mixotrophy.