Plasticity of transcriptional machinery in bacteria is increased by the repertoire of regulatory families

Abstract

Escherichia coli K12 and Bacillus subtilis 168 are two of the best characterized bacterial organisms with a long history in molecular biology for understanding various mechanisms in prokaryotic species. However, at the level of transcriptional regulation little is known on a comparative scale. Here we address the question of the degree to which transcription factors (TFs) and their evolutionary families are shared between them. We found that 59 proteins and 28 families are shared between these two bacteria, whereas different subsets were lineage specific. We demonstrate that majority of the common families expand in a lineage-specific manner. More specifically, we found that AraC, ColD, Ebp, LuxR and LysR families are over-represented in E. coli, while ArsR, AsnC, MarR, MerR and TetR families have significantly expanded in B. subtilis. We introduce the notion of regulatory superfamilies based on an empirical number of functional categories regulated by them and show that these families are essentially different in the two bacteria. We further show that global regulators seem to be constrained to smaller regulatory families and generally originate from lineage-specific families. We find that although TF families may be conserved across genomes their functional roles might evolve in a lineage-specific manner and need not be conserved, indicating convergence to be an important phenomenon involved in the functional evolution of TFs of the same family. Although topologically the networks of transcriptional interactions among TF families are similar in both the genomes, we found that the players are different, suggesting different evolutionary origins for the transcriptional regulatory machinery in both bacteria. This study provides evidence from complete repertoires that not only novel families originate in different lineages but conserved TF families expand/contrast in a lineage-specific manner, and suggests that part of the global regulatory mechanisms might originate independently in different lineages.