Asymmetric divergence of genome organization and transcription beyond LUCA

It is generally assumed that the transcriptional apparatus exhibits a deep divergence across the three domains of life, both for transcription initiation and regulation. The archaeal-type transcription initiation is shared with Eukaryotes, while bacterial transcription initiation presents a simpler architecture. At the same time, transcriptional regulation is shared across Archaea and Bacteria, while Eukaryotes possess a number of distinct regulator protein families absent from the other two domains. This contrasting pattern of transcription-associated protein family distribution is a riddle, connected with the deep, domain-level phylogeny leading to LUCA. By focusing on the few shared transcriptional components, we show that they are all present in Archaea, with marked differences in the other domains, some of which might be bridged with sensitive sequence comparisons. The histone fold and the Lrp domain are detectable in Bacteria and Eukaryotes, respectively - thus limiting salient differences to transcription initiation only. We posit that the bacterial branch has diverged significantly, with rapid evolution connected with an always-on transcription, suggesting that transcription in Archaea might be closer to the root, challenging current views on deep phylogeny and explaining the domain diversification, also supported by parallel evidence such as translation and lipid structure.