Repeat sequences limit the effectiveness of lateral gene transfer and favored the evolution of meiotic sex in early eukaryotes

Abstract

The transition from prokaryotic lateral gene transfer to eukaryotic meiotic sex is poorly understood. Phylogenetic evidence suggests that it was tightly linked to eukaryogenesis, which involved an unprecedented rise in both genome size and the density of genetic repeats. Expansion of genome size raised the severity of Muller’s ratchet, while limiting the effectiveness of lateral gene transfer (LGT) at purging deleterious mutations. In principle, an increase in recombination length combined with higher rates of LGT could solve this problem. Here, we show using a computational model that this solution fails in the presence of genetic repeats prevalent in early eukaryotes. The model demonstrates that dispersed repeat sequences allow ectopic recombination, which leads to the loss of genetic information and curtails the capacity of LGT to prevent mutation accumulation. Increasing recombination length in the presence of repeat sequences exacerbates the problem. Mutational decay can only be resisted with homology along extended sequences of DNA. We conclude that the transition to homologous pairing along linear chromosomes was a key innovation in meiotic sex, which was instrumental in the expansion of eukaryotic genomes and morphological complexity.

The overlooked evolutionary dynamics of 16S rRNA revises its role as the “gold standard” for bacterial species identification

“…This is particularly evident in the aforementioned prokaryotic genus Thermococcus, which, despite expectations, shows one of the lowest diversifications at the 16S rRNA level. And it is mainly extremophilic organisms in which HGT is often mentioned not only as a means of adaptation, but especially as a necessity for maintaining genome integrity 25 , 47 . In general, it is known that the susceptibility of different bacterial genera to HGT varies and is probably related to their life-history traits 48 .…”

“…Particularly for this type of sequence, which is typically found in multiple copies in a genome, the availability of a complete genome sequence is crucial for HGT evaluation, which has been facilitated by the advent of third-generation sequencing technologies and platforms 24 . On the other hand, difficult-to-detect HGT within a bacterial species or between closely related species is probably an important driving force in the evolution of microorganisms 25 . Recently, some studies have emphasized that 16S rRNA, especially in a phylogenetic reconstruction/estimation context, provides inaccurate results, suggesting the involvement of HGT 26 – 28 .…”

Endosymbiotic selective pressure at the origin of eukaryotic cell biology

“…Meiosis in itself is ancient, ubiquitous, and the central process that imparts an advantage to sex in eukaryotes ( Colnaghi et al, 2022 ; Colnaghi et al, 2020 ; Malik et al, 2008 ; Speijer et al, 2015 ). Several theories place mito-nuclear interactions, heteroplasmy, and mitochondrial ROS as drivers of eukaryotic sex ( Colnaghi et al, 2020 ; Hörandl and Speijer, 2018 ; Radzvilavicius and Blackstone, 2015 ).…”

“…Several theories place mito-nuclear interactions, heteroplasmy, and mitochondrial ROS as drivers of eukaryotic sex ( Colnaghi et al, 2020 ; Hörandl and Speijer, 2018 ; Radzvilavicius and Blackstone, 2015 ). HGT alone was insufficient for LECA to escape Mullers ratchet in the absence of homologous recombination ( Colnaghi et al, 2022 ), when considering expanding genome size and repeat sequence frequency. Everything points to an origin of sex and meiosis necessitated by the presence of mitochondria.…”

The rise of complex life

“…Besides bioenergetic constraints, using horizontal gene transfer in prokaryotes instead of sex places constraints on genome size (Colnaghi et al, 2020), especially in case of repeat sequences (Colnaghi et al, 2022) like transposable elements (van Dijk et al, 2022). According to these analyses, the invention of meiotic sex would have enabled the increase in proto-eukaryotic genome size (Colnaghi et al, 2020(Colnaghi et al, , 2022van Dijk et al, 2022). Some complex cellular features, however, are present in certain prokaryotes.…”