Investigation of the Effects of Unusual Genome Architecture on the Evolution of the Ciliate Tetrahymena Using Computational Modeling

Tetraymena is a model organism in molecular biology and has a very unusual genome architecture, including nuclear dimorphism, amitotic division of the somatic nucleus during asexual reproduction, capability to control the copy number of chromosomes during amitosis and the ability to have facultative sex when a germline nucleus is present. Recent studies also revealed that Tetrahymena has very special evolutionary characteristics, such as the prevalence of successful asexuality within the genus and the extremely low mutation rate found in the germline nucleus. How Tetrahymena evolves such unusual characteristics is still unclear, and whether and how the unusual genome architecture contributes to the unusual evolutionary characteristics remain largely untested or uninvestigated. In this study, I investigated the effect of these unusual genome features on the evolution of Tetrahymena using computational modeling, particularly on their contributions to their successful asexuality and the extremely low mutation rate. I found that compared to mitosis, amitosis of somatic nucleus, together with copy number control, can both decelerate the operation of Muller’s ratchet to a sexual-comparable extent and speed up the adaptation to changing environments. I also found that although not expressed during asexual generations, the mutations arising in the germline nucleus can also respond to selection acting on the somatic nucleus following sexual reproduction, which rejects the previous explanation for the low germline nucleus mutation rate in Tetrahymena. Instead, my results showed that the reproduction strategies adopted by Tetrahymena, including amitosis and facultative sex, can naturally promote the reduction of mutation rate under selection. This study highlighted the contribution of unusual genome architecture to the achievement of unusual evolutionary characteristics found in Tetrahymena, which both lead to a better understanding of the evolution of this organism and elucidate new mechanisms for eukaryotes to survive asexually and promote mutation rate reduction.