Opinion: Genetic Conflict With Mobile Elements Drives Eukaryotic Genome Evolution, and Perhaps Also Eukaryogenesis

Abstract

Through analyses of diverse microeukaryotes, we have previously argued that eukaryotic genomes are dynamic systems that rely on epigenetic mechanisms to distinguish germline (i.e., DNA to be inherited) from soma (i.e., DNA that undergoes polyploidization, genome rearrangement, etc.), even in the context of a single nucleus. Here, we extend these arguments by including two well-documented observations: (1) eukaryotic genomes interact frequently with mobile genetic elements (MGEs) like viruses and transposable elements (TEs), creating genetic conflict, and (2) epigenetic mechanisms regulate MGEs. Synthesis of these ideas leads to the hypothesis that genetic conflict with MGEs contributed to the evolution of a dynamic eukaryotic genome in the last eukaryotic common ancestor (LECA), and may have contributed to eukaryogenesis (i.e., may have been a driver in the evolution of FECA, the first eukaryotic common ancestor). Sex (i.e., meiosis) may have evolved within the context of the development of germline-soma distinctions in LECA, as this process resets the germline genome by regulating/eliminating somatic (i.e., polyploid, rearranged) genetic material. Our synthesis of these ideas expands on hypotheses of the origin of eukaryotes by integrating the roles of MGEs and epigenetics.

Keywords: LECA; epigenetics; eukaryotic diversity; meiosis; transposable elements; viruses.

Figure 1.

Genetic conflict during eukaryogenesis resulted in epigenetically regulated germline–soma distinctions in eukaryotes. This figure depicts the players at the origin of eukaryotes, namely the diversity of viruses and the presence of TEs integrated within both bacteria, including the ancestor of mitochondria, and archaea, including the likely host cell of FECA (top panel). Conflict among these genomes and mobile genetic elements (MGEs; middle panel) resulted in eukaryotes that distinguish germline (i.e., marked for inheritance, capable of meiosis to reset genome, represented by the condensed chromosomes in LECA) and somatic (e.g., cyclical polyploidy, extrachromosomal DNA, developmentally regulated genome rearrangements, DNA elimination, represented by the thinner lines within the nucleus of LECA) material (bottom panel). The inset under the somatic functions in LECA represents three somatic chromosomes generated from a single germline region in the ciliate Chilodonella uncinata (redrawn from Gao et al. 2015). Additional details and references can be found in the text.