Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origin

Abstract

Establishing a unified timescale for the early evolution of Earth and life is challenging and mired in controversy because of the paucity of fossil evidence, the difficulty of interpreting it and dispute over the deepest branching relationships in the tree of life. Surprisingly, it remains perhaps the only episode in the history of life where literal interpretations of the fossil record hold sway, revised with every new discovery and reinterpretation. We derive a timescale of life, combining a reappraisal of the fossil material with new molecular clock analyses. We find the last universal common ancestor of cellular life to have predated the end of late heavy bombardment (>3.9 billion years ago (Ga)). The crown clades of the two primary divisions of life, Eubacteria and Archaebacteria, emerged much later (<3.4 Ga), relegating the oldest fossil evidence for life to their stem lineages. The Great Oxidation Event significantly predates the origin of modern Cyanobacteria, indicating that oxygenic photosynthesis evolved within the cyanobacterial stem lineage. Modern eukaryotes do not constitute a primary lineage of life and emerged late in Earth's history (<1.84 Ga), falsifying the hypothesis that the Great Oxidation Event facilitated their radiation. The symbiotic origin of mitochondria at 2.053-1.21 Ga reflects a late origin of the total-group Alphaproteobacteria to which the free living ancestor of mitochondria belonged.

No genome is an island: toward a 21st century agenda for evolution

“…Bacteria and archaea are the oldest evolutionary lineages (>3.4 GYA) and show the broadest metabolic diversity, inhabiting all planetary environments , . We know nothing about their origins.…”

“…The ancestor of all eukaryotic cells, in contrast, arose less than 1.8 GYA following an endosymbiogenetic merger of an aerobic proteobacterium and an unknown but advanced archaeal cell . This conclusion is based on two kinds of observations: DNA evidence shows that all known eukaryotes, with a single exception, carry mitochondria or mitochondrion‐derived organelles .…”

“…16 Bacteria and archaea are the oldest evolutionary lineages (>3.4 GYA) and show the broadest metabolic diversity, inhabiting all planetary environments. k, 17,18 We know nothing about their origins. Nonetheless, the parallel use of DNA, RNA, and proteins as carriers and expression products of hereditary code by both prokaryotic cell types indicates shared ancestry at some unknown primordial stage of life history.…”

“…The ancestor of all eukaryotic cells, in contrast, arose less than 1.8 GYA following an endosymbiogenetic merger of an aerobic proteobacterium and an unknown but advanced archaeal cell. 18,19 This conclusion is based on two kinds of observations: i http://shapiro.bsd.uchicago.edu/No_Genome_is_an_ Island_Extra_References_4.html j http://shapiro.bsd.uchicago.edu/Key_Scientists_ Advocating_non-Gradualist_Evolution_in_the_19th_ and_20th%20Centuries.html k http://shapiro.bsd.uchicago.edu/No_Genome_is_an_ Island_Extra_References_4.html r DNA evidence shows that all known eukaryotes, with a single exception, carry mitochondria or mitochondrion-derived organelles. 20 These organelles have small genomes encoding ribosomal RNA molecules that indicate a unique evolutionary ancestry, closely related to the ␣-Proteobacteria, known to reproduce inside eukaryotic cells, and also to recently described marine Proteobacteria.…”

Molecular function limits divergent protein evolution on planetary timescales

“…Based on the recently proposed affiliation of eukaryotes and members from the Lokiarchaeota [64], divergence times between S. solfataricus and eukaryotes were set at 2.7 billion years, i.e. the estimated age of the TACK superphylum [65,66].…”