Revisiting the hypothesis of an energetic barrier to genome complexity between eukaryotes and prokaryotes

Abstract

The absence of genome complexity in prokaryotes, being the evolutionary precursors to eukaryotic cells comprising all complex life (the prokaryote–eukaryote divide), is a long-standing question in evolutionary biology. A previous study hypothesized that the divide exists because prokaryotic genome size is constrained by bioenergetics (prokaryotic power per gene or genome being significantly lower than eukaryotic ones). However, this hypothesis was evaluated using a relatively small dataset due to lack of data availability at the time, and is therefore controversial. Accordingly, we constructed a larger dataset of genomes, metabolic rates, cell sizes and ploidy levels to investigate whether an energetic barrier to genome complexity exists between eukaryotes and prokaryotes while statistically controlling for the confounding effects of cell size and phylogenetic signals. Notably, we showed that the differences in bioenergetics between prokaryotes and eukaryotes were less significant than those previously reported. More importantly, we found a limited contribution of power per genome and power per gene to the prokaryote–eukaryote dichotomy. Our findings indicate that the prokaryote–eukaryote divide is hard to explain from the energetic perspective. However, our findings may not entirely discount the traditional hypothesis; in contrast, they indicate the need for more careful examination.

The role of mitochondrial energetics in the origin and diversification of eukaryotes

“…Because the energy demands of cells (i.e., ATP requirements and maximum metabolic rates (10,19)) scale continuously and nearly linearly with volume, and prokaryotes and eukaryotes overlap across this continuum (Fig. 2A), such comparisons between rough averages are misleading.…”

“…The goal here is to isolate the genomic design of a cell from other confounding factors that also separate eukaryotes from prokaryotes. Because ATP demands depend on cell volume (and not complexity or gene number (10,19)), we considered the amount of ATP that remains (1 − 𝑐 𝐷𝑁𝐴,𝑒𝑢𝑘 and 1 − 𝑐 𝐷𝑁𝐴,𝑝𝑟𝑜𝑘 ) after accounting for the relative cost of DNA that is associated with each genomic design (𝑐 𝐷𝑁𝐴,𝑒𝑢𝑘 and 𝑐 𝐷𝑁𝐴,𝑝𝑟𝑜𝑘 ; Fig. 4 and Eq.…”

“…Mitochondria are the cause of these massive energetic differences, Lane and Martin argue, and were thus a pre-requisite for the evolution of the eukaryotic complexity (3,18). Marinov (10), and Chiyomaru and Takemoto (19). Unlike in B, the cell volume of prokaryotes is constrained.…”

“…Some authors have expressed skepticism about the energetic hypothesis for the origin of eukaryotic complexity (10,(19)(20)(21)(22)(23)(24). The notion that the evolution of cell complexity requires an increased energy supply has been dismissed as having no evolutionary basis (22,24), and the concept of 'energy per gene' has been criticized as evolutionarily meaningless (23,25).…”

Metabolic allometry: A genomic approach to scaling

“…It is easy to fall into the discussion of the effect of a nucleotide more or less in the code can generate big changes, however, it is necessary to take into account that any energy analysis methodology like ours, must take into account that the energy cost of genomes with more and less complex structures are similar because always follow a power-law relationship (Lynch and Marinov, 2015), where the growth requirements per cell scale with cell volume in a power-law relationship with highly significant regression (r 2 near to 1) indicating a linear relationship between the energetic requirement for growth and cell volume that involve for example, the same pattern when compare prokaryotic and eukaryotic cells (Lynch andMarinov, 2015, Chiyomaru &Takemoto, 2020). This example, implies that any overweight of importance of specific components of genomes in the energy expenditure invokes an, unlike variable metabolic scaling.…”