Gene duplications trace mitochondria to the onset of eukaryote complexity

Abstract

The last eukaryote common ancestor (LECA) lived 1.6 billion years ago1,2. It possessed nuclei, sex, an endomembrane system, mitochondria, and all key traits that make eukaryotic cells more complex than their prokaryotic ancestors2-6. The closest known relatives of the host lineage that acquired the mitochondrion are, however, small obligately symbiotic archaea that lack any semblance of eukaryotic cell complexity7. Although the steep evolutionary grade separating prokaryotes from eukaryotes increasingly implicates mitochondrial symbiosis at eukaryote origin4,7, the timing and evolutionary significance of mitochondrial origin remains debated. Gradualist theories contend that eukaryotes arose from archaea by slow accumulation of eukaryotic traits8-10 with mitochondria arriving late11, while symbiotic theories have it that mitochondria initiated the onset of eukaryote complexity in a non-nucleated archaeal host7 by gene transfers from the organelle4,12-14. The evolutionary process leading to LECA should be recorded in its gene duplications. Among 163,545 duplications in 24,571 gene trees spanning 150 sequenced eukaryotic genomes we identified 713 gene duplication events that occurred in LECA. LECAs bacterially derived genes were duplicated more frequently than archaeal derived or eukaryote specific genes, reflecting the serial copying15,16 of genes from the mitochondrial endosymbiont to the archaeal hosts chromosomes prior to the onset of eukaryote genome complexity. Bacterial derived genes for mitochondrial functions, lipid synthesis, biosynthesis, as well as core carbon and energy metabolism in LECA were duplicated more often than archaeal derived genes and even more often than eukaryote-specific inventions for endomembrane, cytoskeletal or cell cycle functions. Gene duplications record the sequence of events at LECAs origin and indicate that recurrent gene transfer from a resident mitochondrial endosymbiont preceded the onset of eukaryotic cellular complexity.