The physiology and habitat of the last universal common ancestor

Abstract

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 6.1 million protein coding genes from sequenced prokaryotic genomes in order to reconstruct the microbial ecology of LUCA. Among 286,514 protein clusters, we identified 355 protein families (∼0.1%) 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 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, coenzyme A, ferredoxin, molybdopterin, corrins and selenium. Its genetic code required nucleoside modifications and S-adenosyl methionine-dependent methylations. The 355 phylogenies identify clostridia and methanogens, whose modern lifestyles resemble that of LUCA, as basal among their respective domains. LUCA inhabited a geochemically active environment rich in H2, CO2 and iron. The data support the theory of an autotrophic origin of life involving the Wood-Ljungdahl pathway in a hydrothermal setting.

Integrative modeling of gene and genome evolution roots the archaeal tree of life

“…It is challenging to map genes to deep nodes in the phylogeny with high probability, and our reconstruction did not allow us to determine whether the electron donor for this reaction was organic or inorganic. Our mapping of the Wood-Ljungdahl pathway to the deepest nodes of the archaeal tree is in agreement with biochemical arguments and recent analyses using different methods (72,73) that have suggested that the reduction of CO 2 with H 2 to produce organic compounds was central to the metabolism of an anaerobic last common ancestor of Bacteria and Archaea. Our analysis also suggests that the LACA had most of the modern archaeal transcription, translation, and DNA replication machineries, components of the exosome and proteasome, a secretion system, and some of the key genes for synthesizing archaeal ether lipids (SI Appendix, Figs.…”

“…The DTL analysis and new root provides inferences of gene content evolution that are consistent with inferences of early archaeal physiology based on other lines of evidence (20,72,73). Our analysis suggests that the LACA was an anaerobe that fixed carbon via the Wood-Ljungdahl pathway, and that adaptations to aerobic metabolism evolved independently across the tree.…”

Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea

“…In order to gain some insight on how ancient is the translation of intraRNAs, we focus on fusA , which encodes for the translational elongation factor 2, a universal protein probably present in the Last Universal Common Ancestor (LUCA) [54,55]. This elongation factor has homologues in all three domains of life: EF-G in bacteria, eEF-2 in eukaryotes and aEF-2 in archaea and is composed of five domains, a GTPase domain and domains II to V [45].…”

Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

“…Thus, older events are inherently more difficult to study. These hurdles make it challenging to piece together not only the evolution of phototrophy but also the origins of the six known carbon fixation pathways (12,13), as they may have been some of the earliest metabolisms to evolve (14)(15)(16)(17)(18). To this end, the antiquity of these metabolisms has hampered efforts to retrace their origins and identify what pathway was used by the earliest photoautotrophs.…”