Phenotypic reconstruction of the last universal common ancestor reveals a complex cell

Abstract

A fundamental concept in evolutionary theory is the last universal common ancestor (LUCA) from which all living organisms. While some authors have suggested a relatively complex LUCA it is still widely assumed that LUCA must have been a very simple cell and that life has subsequently increased in complexity through time. However, while current thought does tend towards a general increase in complexity through time in Eukaryotes, there is increasing evidence that bacteria and archaea have undergone considerable genome reduction during their evolution. This raises the surprising possibility that LUCA, as the ancestor of bacteria and archaea may have been a considerably complex cell. While hypotheses regarding the phenotype of LUCA do exist, all are founded on gene presence/absence. Yet, despite recent attempts to link genes and phenotypic traits in prokaryotes, it is still inherently difficult to predict phenotype based on the presence or absence of genes alone. In response to this, we used Bayesian phylogenetic comparative methods to predict ancestral traits. Testing for robustness to horizontal gene transfer (HGT) we inferred the phenotypic traits of LUCA using two robust published phylogenetic trees and a dataset of 3,128 bacterial and archaeal species (Supplementary Information). Our results depict LUCA as a far more complex cell than has previously been proposed, challenging the evolutionary model of increased complexity through time in prokaryotes. Given current estimates for the emergence of LUCA we suggest that early life very rapidly evolved considerable cellular complexity.

A rooted phylogeny resolves early bacterial evolution

“…4). We also identified most of the proteins required for flagella and pili synthesis and those for quorum sensing, sug-gesting that LBCA was motile (51,52). Given that bacterial genes are typically maintained by strong purifying selection (53), these findings imply that LBCA lived in an environment in which dispersal, chemotaxis, and surface attachment were advantageous.…”

“…Moderate support for the presence of the shape-determining protein mreB (0.9/0.88/0.73, root branches 1-3 as depicted in Fig. 1B), mreC (0.82/0.79/0.57) and mreD (0.86/0.83/0.63) at the root suggests that LBCA were rod-shaped cells (52). We also obtained high root PPs for proteins mediating outer cell envelope biosynthesis including lipopolysaccharides (LPS), from which we infer that LBCA had a double membrane with an LPS layer (36).…”

Origins of Life: Chemistry and Evolution

“…Today, that quest is focused on the scientific search for the origin of life itself. We now know that the backbones and sidechains of life's essential biopolymers -RNA, DNA, and polypeptide -were fixed in chemical structure at the time of the last universal common ancestor, nearly four billion years ago (1)(2)(3)(4), and that they have been held invariant over all biological time and all speciation. Thus, the origins of biopolymers embody the central question about the origin of life.…”

Origins of Life: Chemistry and Evolution

“…Today, that quest is focused on the scientific search for the origin of life itself. We now know that the backbones and sidechains of life's essential biopolymers, RNA, DNA, and polypeptide were fixed in chemical structure by the time of the last universal common ancestor, around four billion years ago (1)(2)(3)(4), and that they have been held invariant over all biological time and all speciation. Thus, the origins of biopolymers embody the central question about the origin of life.…”