IN SEARCH OF MICROBE NUMBER ONE

The concept of a last universal common ancestor of all cells (LUCA, or the progenote) is central to the study of early evolution and life`s origin, yet information about how and where LUCA lived is lacking. We investigated all clusters and phylogenetic trees for all protein coding genes from 2000 sequenced prokaryotic genomes in order to reconstruct the microbial ecology of LUCA. Among 286,514 protein clusters constructed, we identified 355 protein families (~0.1% of the total) that trace to LUCA by phylogenetic criteria. Because these proteins are not universally distributed, they can shed light on LUCA`s physiology. Their functions, properties, and prosthetic groups depict LUCA as anaerobic, CO₂-fixing, H₂-dependent with a Wood-Ljungdahl (WL) pathway, N₂-fixing, and thermophilic. LUCA`s biochemistry was replete with FeS clusters and radical reaction mechanisms. Its cofactors reveal dependence upon transition metals, flavins, S-adenosyl methionine (SAM), coenzyme A, ferredoxin, molybdopterin, corrins, and selenium. Its genetic code required nucleoside modifications and SAM-dependent methylations. The 355 phylogenies identify clostridia and methanogens, whose modern lifestyles resemble LUCA`s, as basal among their respective domains. LUCA inhabited a geochemically active environment rich in H₂, CO₂, and iron. The data indicate that the first organic molecules — and life — arose from CO₂ in a hydrothermal settings and find independent support from new laboratory work demonstrating the facile synthesis of intermediates and endproducts of the WL pathway from native metals, water and CO₂. It appears that LUCA lived from exergonic reactions of gasses with transition metals and water, reactions that generated soluble organic compounds and permitted the harnessing of chemical energy as thioestes and acyl phophates that could perform metabolic work.