Limits to the cellular control of sequestered cryptophyte prey in the marine ciliate Mesodinium rubrum

Abstract

The marine ciliate <i>Mesodinium rubrum</i> is famous for its ability to acquire and exploit chloroplasts and other cell organelles from some cryptophyte algal species. We sequenced genomes and transcriptomes of free-swimming <i>Teleaulax amphioxeia</i>, as well as well-fed and starved <i>M. rubrum</i> in order to understand cellular processes upon sequestration under different prey and light conditions. From its prey, the ciliate acquires the ability to photosynthesize as well as the potential to metabolize several essential compounds including lysine, glycan, and vitamins that elucidate its specific prey dependency. <i>M. rubrum</i> does not express photosynthesis-related genes itself, but elicits considerable transcriptional control of the acquired cryptophyte organelles. This control is limited as light-dependent transcriptional changes found in free-swimming <i>T. amphioxeia</i> got lost after sequestration. We found strong transcriptional rewiring of the cryptophyte nucleus upon sequestration, where 35% of the <i>T. amphioxeia</i> genes were significantly differentially expressed within well-fed <i>M. rubrum</i>. Qualitatively, 68% of all genes expressed within well-fed <i>M. rubrum</i> originated from <i>T. amphioxeia</i>. Quantitatively, these genes contributed up to 48% to the global transcriptome in well-fed <i>M. rubrum</i> and down to 11% in starved <i>M. rubrum</i>. This tertiary endosymbiosis system functions for several weeks, when deprived of prey. After this point in time, the ciliate dies if not supplied with fresh prey cells. <i>M. rubrum</i> represents one evolutionary way of acquiring photosystems from its algal prey, and might represent a step on the evolutionary way towards a permanent tertiary endosymbiosis.