Transcriptomic analyses reveal sexual cues in reproductive life stages of uncultivated Acantharia (Radiolaria)

The ability to reproduce is a key process for the perpetuation of organisms. Along the evolution of protist reproductive strategies, the molecular machinery of sexual recombination is estimated to have been inherited from the last eukaryotic common ancestor (LECA). Unraveling the sexual cycles of free-living protists remains challenging, given the enigmatic roles of many uncultivated life stages. For the planktonic group of Acantharia (Radiolaria), a hypothetical sexual cycle has been proposed since the late 19th century, including a gamete-like stage, referred to as swarmers. In order to investigate the sexual nature of acantharian reproductive stages, we compared transcriptomes of various acantharian life stages. Our results show distinct functional profiles for reproductive and vegetative stages, while revealing the expression of the gamete fusion genes, HAP2/GCS1 and KAR5-GEX1-BMB in swarmers. Annotation of differentially expressed life stage-specific genes, also highlighted putative meiosis-related functions among pre-swarmer and swarmer stages, while suggesting the existence of a putative zygotic stage. This original life stage-specific genetic data is coherent with morphological evidence supporting the acantharian sexual cycle, with swarmers acting as gametes. Moreover, it paves the way for a deeper understanding of radiolarian cell biology and ecology at a single-cell scale.