On the origin of genomes and cells within inorganic compartments

Abstract

Building on the model of Russell and Hall for the emergence of life at a warm submarine hydrothermal vent, we suggest that, within a hydrothermally formed system of contiguous iron-sulfide (FeS) compartments, populations of virus-like RNA molecules, which eventually encoded one or a few proteins each, became the agents of both variation and selection. The initial darwinian selection was for molecular self-replication. Combinatorial sorting of genetic elements among compartments would have resulted in preferred proliferation and selection of increasingly complex molecular ensembles--those compartment contents that achieved replication advantages. The last universal common ancestor (LUCA) we propose was not free-living but an inorganically housed assemblage of expressed and replicable genetic elements. The evolution of the enzymatic systems for (i) DNA replication; and (ii) membrane and cell wall biosynthesis, enabled independent escape of the first archaebacterial and eubacterial cells from their hydrothermal hatchery, within which the LUCA itself remained confined.

Figure 1

A scenario of evolution from the origin of RNA molecules to the independent escape of archaebacterial and eubacterial cells within naturally forming inorganic compartments consisting primarily of FeS at a Hadean (>3.8 Ga old) hydrothermal vent. The left hand side of the figure shows the proposed sequence of events (from the bottom to the top) described in the main text; the right portion is a highly schematic drawing illustrating increasingly complex levels of molecular organization within the compartments along the path from inorganic carbon to LUCA and from LUCA to free-living chemoautotrophic prokaryotes (modified from Ref. [24]). The enlarged compartment shows the proposed retrovirus-like genetic cycle of LUCA . The synthesis of the RNA–DNA hybrid and the dsDNA is thought to have been catalyzed by reverse transcriptase, with RNase H (a ubiquitous, probably, ancestral enzyme) involved in RNA strand removal during the latter step. The transcription of RNA from dsDNA would have been catalyzed by DNA-dependent RNA polymerase (another universal enzyme). The parts of the replication system that are shared by archaebacteria and eubacteria (sliding clamp, clamp loader ATPase and DNA ligase) might have been involved in the dsDNA synthesis and/or transcription steps. The figure is schematic, and not drawn to scale. The compartments could be from <1–100 μm in diameter, as in fossil and modern vents (see main text for details).