Integration and regulation of stolen organelles in a marine protist

Abstract

Chloroplast-stealing (a.k.a., “kleptoplastidic”) plankton transiently obtain and integrate prey metabolic machinery into their own cells. To do so, they must address a series of challenges, including physical localization of acquired machinery, metabolic integration of organelles and their products, and maintenance of machinery. Here, we study this transient integration in the marine ciliate Mesodinium chamaeleon by pulse feeding the ciliate with cryptophyte algal prey (Storeatula major) and then tracking changes in ciliate cellular ultrastructure, physiology (growth and photosynthesis), and gene expression over time. We demonstrate a predictable series of changes, from the reconfiguration of metabolic activity fueled by recent ingestion, to a period of rapid growth, to a reduction in physiological performance as prey organelle number and functionality become limiting. Because M. chamaeleon also steals transcriptionally active prey nuclei, gene expression is a complex milieu of host and cryptophyte expression, with much of prey metabolism apparently intact in the new host, albeit at low levels. Collectively, our results highlight the holistic orchestration of stolen organelles to produce rapid—yet transient—growth in a new host.