Diverse Genome Structures among Eukaryotes May Have Arisen in Response to Genetic Conflict

Abstract

In contrast to the typified view of genome cycling only between haploidy and diploidy, there is evidence from across the tree of life of genome dynamics that alter both copy number (i.e. ploidy) and chromosome complements. Here, we highlight examples of such processes, including endoreplication, aneuploidy, inheritance of extrachromosomal DNA, and chromatin extrusion. Synthesizing data on eukaryotic genome dynamics in diverse extant lineages suggests the possibility that such processes were present before the last eukaryotic common ancestor. While present in some prokaryotes, these features appear exaggerated in eukaryotes where they are regulated by eukaryote-specific innovations including the nucleus, complex cytoskeleton, and synaptonemal complex. Based on these observations, we propose a model by which genome conflict drove the transformation of genomes during eukaryogenesis: from the origin of eukaryotes (i.e. first eukaryotic common ancestor) through the evolution of last eukaryotic common ancestor.

Keywords: aneuploidy; eukaryogenesis; genetic conflict; genome dynamics; meiosis; polyploidy.

Fig. 1.

Examples of diverse microbial eukaryotes discussed in parts I and II. a) Ammonia (Rhizaria, Foraminifera), isolated in our lab; b) Aulacantha (Rhizaria, formerly radiolaria); c) Giardia (“Excavata”); d) Naviculoid diatom (Stramenopila); e) Acanthamoeba (Amoebozoa); f) Oxytricha (Alveolata, Ciliophora). Images b)–f) accessed from the internet and all available under CC3 license.

Fig. 2.

Taxonomy of organisms discussed with eukaryotes (purple) shown as nested among the archaea (blue) and sister to bacteria (red). We document genomic features associated with instability that are present throughout the tree of life, particularly among eukaryotes (see part I). The tree is rooted on opisthokonts as suggested by Cerón-Romero et al. (2022), though this is controversial; an alternative hypothesis is that the root lies among the “Excavata” (taxon in quotes as monophyly unclear; Al Jewari and Baldauf 2023). Absences of a feature may represent a lack of data (common among microeukaryotes) rather than true absences. Colored boxes on the tree encircle monophyletic clades. G, growth; M, multinucleate; *, somatic. As discussed in the text, the question mark indicates the inferences of polyploidy in Asgard (and other) archaea. Arrow points to the FECA to LECA transition (i.e. eukaryogenesis) as discussed in the text.

Fig. 3.

Examples of noncanonical chromatin dynamics in diverse lineages, which suggest a division between germline and somatic material within nuclei. a) Chromatin elimination from soma in the form of B chromosomes and from the germline as occurs during paternal germline elimination in some insects (see Dedukh and Krasikova 2022). b) Extrusion of compact chromatin in A. proteus based on images from Goodkov et al. (2020). c) Fission of genetic material in Cochliopodium, with purple representing the DAPI stained nucleus from Tekle et al. (2014). d) Zerfall, in Allogromia laticollaris (Foraminifera); here, DNA at an estimated 11,000 N is extruded throughout the cytoplasm prior to the formation of gametic nuclei; illustration based on Timmons et al. (2024). Artwork by Tejasvi Kumaran (Smith College).

Fig. 4.

Our hypothesis on the role of genetic conflict during eukaryogenesis (i.e. the FECA to LECA transition), including in driving genome structures and ultimately the evolution of karyotypes. We propose that eukaryotic innovations arose as a response to the conflict between genomes plus an influx of MGEs (e.g. transposable elements [green] and viruses) at the fusion of a bacterium (orange) and an archaeon (blue), which led to both intra- and intergenomic conflict. Conflict within chromosomes led to the evolution of both telomeres and centromeres (see text part I; left panel) as well as an expansion of mechanisms for gene conversion that can remove deleterious alleles. We speculate that early eukaryotes divided genetic material randomly through amitosis (see Table 1) and that subsequent competition among chromosomes resulted in the evolution of centromeres that compete for spindle fibers (middle panel). At some point, eukaryotes evolved nuclei (purple dashed circle) along with mechanisms to distinguish germline (inherited) from somatic (expressed) genetic material, and that the concomitant evolution of the synaptonemal complex enabled the establishment of karyotypes and subsequently the evolution of biological species (i.e. those that are reproductively isolated; right panel). These processes led to a complex LECA (far right image), likely an amoeboflagellate that could grow (by either increasing nuclear size and/or becoming multinucleated), fuse, and divide. Under such a scenario, the dynamic features observed among extant eukaryotes (Figs. 2 and 3) likely build from a combination of ancestral and recently evolved features that regulate distinctions between germline (i.e. carrying epigenetic marks) and somatic (i.e. polyploid, aneuploid, extrachromosomal/extruded DNA) genetic material.