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

Abstract

The origin of eukaryotic cell size and complexity is thought by some to have required an energy excess provided by mitochondria, whereas others claim that mitochondria provide no energetic boost to eukaryotes. Recent observations show that energy demand scales continuously and linearly with cell volume across both prokaryotes and eukaryotes, and thus suggest that eukaryotes do not have an increased energetic capacity over prokaryotes. However, amounts of respiratory membranes and ATP synthases scale super-linearly with cell surface area. Furthermore, the energetic consequences of the contrasting genomic designs between prokaryotes and eukaryotes have yet to be precisely quantified. Here, we investigated (1) potential factors that affect the cell volumes at which prokaryotes become surface area-constrained, and (2) the amount of energy that is divested to increasing amounts of DNA due to the contrasting genomic designs of prokaryotes and eukaryotes. Our analyses suggest that prokaryotes are not necessarily constrained by their cell surfaces at cell volumes of 10⁰‒10³ μm³, and that the genomic design of eukaryotes is only slightly advantageous at genomes sizes of 10⁶‒10⁷ bp. This suggests that eukaryotes may have first evolved without the need for mitochondria as these ranges hypothetically encompass the Last Eukaryote Common Ancestor and its proto-eukaryotic ancestors. However, our analyses also show that increasingly larger and fast-dividing prokaryotes would have a shortage of surface area devoted to respiration and would disproportionally divest more energy to DNA synthesis at larger genome sizes. We thus argue that, even though mitochondria may not have been required by the first eukaryotes, the successful diversification of eukaryotes into larger and more active cells was ultimately contingent upon the origin of mitochondria.