Abstract

Author Summary Tetrahymena thermophila is a single-celled organism with seven sexes. After two cells of different sexes mate, the progeny cells can be of any one of the seven sexes. In this article we show how this sex decision is made. Every cell has two genomes, each contained within a separate nucleus. The germline genome is analogous to that in our ovaries or testes, containing all the genetic information for the sexual progeny; the somatic or working genome controls the operation of the cell (including its sex). We show that the germline genome contains a tandem array of similarly organized but incomplete gene pairs, one for each sex. Sex is chosen after fertilization when a new somatic genome is generated by rearrangement of a copy of the germline genome. One complete sex gene pair is assembled when the cell joins DNA segments at opposite ends of the array to each end of one incomplete gene pair; this gene pair is thus completed and becomes fully functional, while the remaining sex gene pairs are excised and lost. The process involves programmed, site-specific genome rearrangements, and the physically independent rearrangements that occur at opposite ends of the selected gene pair happen with high reliability and precision.

Highlights

  • Unicellular eukaryotes reproduce asexually, but most have a sexual stage to their life cycle that increases genotypic variability

  • This discovery initiated the field of microbial genetics, as mating types were subsequently found in bacteria and a diversity of microbial eukaryotes

  • The germline genome is analogous to that in our ovaries or testes, containing all the genetic information for the sexual progeny; the somatic or working genome controls the operation of the cell

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Summary

Introduction

Unicellular eukaryotes reproduce asexually, but most have a sexual stage to their life cycle that increases genotypic variability. Mating types were first discovered by Sonneborn in the ciliate Paramecium aurelia [1]. This discovery initiated the field of microbial genetics, as mating types were subsequently found in bacteria and a diversity of microbial eukaryotes. During conjugation (Figure S1) the parental somatic nucleus is destroyed while new somatic and germline nuclei are differentiated from a zygote nucleus. This differentiation includes extensive site-specific genome rearrangements, including fragmentation of the germline chromosomes, de novo telomere addition, and deletion of thousands of internal eliminated sequences (IESs) [7]. Mating type is determined at this stage [8]

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