An integrated framework for evolution of ciliated protists (Protista, Ciliophora) from the perspective of comparative genomics

Abstract

Early-branching eukaryotes are associated with the early branching events during eukaryogenesis. Understanding their genomic diversity and evolution can provide insights into the origin and speciation of eukaryotes. Ciliated protists (ciliates) are a group of early-branching unicellular eukaryotes with a high biodiversity, making them excellent models for evolutionary studies. However, their genomic diversity and evolution remain insufficiently understood. In this study, the comparative genomic and phylogenomic analyses were conducted using well-annotated macronuclear genomes from 16 bulk-cultured ciliates across four major classes. Our results indicate that: a) ciliates exhibit significant genomic diversity, with genome sizes ranging from 18.4 Mb to 117.1 Mb, extensive stop codon rearrangements, and tens of thousands of nanochromosomes in Spirotrichea and Litostomatea, reflecting dynamic genome architecture and adaptive evolution; b) gene family expansions highlight divergent evolutionary trajectories among ciliate classes, with Heterotrichea enhancing cell division capacity and Spirotrichea focusing on signal transduction; c) phylogenetic and structural analyses of meiosis related zinc finger protein and calcium channel related calmodulin gene families indicate that they predate the divergence of ciliates with functional diversification; d) anaerobic Entodinium caudatum retains abundant ubiquitin-related genes, while halotolerant Fabrea salina enriches anaphase-promoting complex cofactors (a crucial E3 ubiquitin ligase), suggesting that the encystment might be enhanced for both species. In summary, we systematically investigated the genomic landscape of ciliates to broaden our understanding of the genomic diversity and evolutionary patterns of ciliates.

Keywords: Adaption; Ciliate; Comparative genomics; Early-branching eukaryotes; Evolution; Genetic diversity.