Decoding the genomic tapestry: evolutionary and functional innovations in extrusome-bearing ciliates (Eukaryota, Alveolata) through multi-species comparative genomics

Extrusomes are membrane-bounded extrusive organelles found in a diversity of ciliated protozoa. These organelles have different structures containing materials that are usually expelled or extruded from the cell to engage in different functions. Previous studies have mainly focused on the ultrastructure, biogenesis, function, and extrusion mechanism of different types of extrusomes in specific ciliates. In contrast, comparative and evolutionary genomic studies among extrusome-bearing ciliates have been largely overlooked. Using omics data from 71 ciliates, we conducted a comparative genomics study focusing onfive ciliate taxa with extrusomes (Tetrahymena, Paramecium, Haptoria, Strombidium, and Euplotes).We recovered the sequences of trichocyst matrix proteins (TMPs) from nine Paramecium speciesand performed the corresponding molecular evolution analyses. Evolutionary history analysis emphasized the integral role of the Cryogenian Ice Age in the evolution of the predatory taxon Haptoria and revealed the effects of the two largest Paleozoic radiations on the biodiversity of Paramecium, Haptoria, and Euplotes. Functional enrichment analyses of significantly expanded gene families in five target ciliate taxa highlighted the importance of genes related to metabolism, transport, catalytic activity, and cell signaling. Most importantly, our findings revealed the functional coordination among different components in processes related to extrusomes. Together, the results presented in this study shed light on the evolutionary and genomic adaptations of ciliates with extrusomes and provide a blueprint for future investigations of extrusome-related behaviors.