Abstract
Reconstruction of the regulatory network is an important step in understanding how organisms control the expression of gene products and therefore phenotypes. Recent studies have pointed out the importance of regulatory network plasticity in bacterial adaptation and evolution. The evolution of such networks within and outside the species boundary is however still obscure. Sinorhizobium meliloti is an ideal species for such study, having three large replicons, many genomes available and a significant knowledge of its transcription factors (TF). Each replicon has a specific functional and evolutionary mark; which might also emerge from the analysis of their regulatory signatures. Here we have studied the plasticity of the regulatory network within and outside the S. meliloti species, looking for the presence of 41 TFs binding motifs in 51 strains and 5 related rhizobial species. We have detected a preference of several TFs for one of the three replicons, and the function of regulated genes was found to be in accordance with the overall replicon functional signature: house-keeping functions for the chromosome, metabolism for the chromid, symbiosis for the megaplasmid. This therefore suggests a replicon-specific wiring of the regulatory network in the S. meliloti species. At the same time a significant part of the predicted regulatory network is shared between the chromosome and the chromid, thus adding an additional layer by which the chromid integrates itself in the core genome. Furthermore, the regulatory network distance was found to be correlated with both promoter regions and accessory genome evolution inside the species, indicating that both pangenome compartments are involved in the regulatory network evolution. We also observed that genes which are not included in the species regulatory network are more likely to belong to the accessory genome, indicating that regulatory interactions should also be considered to predict gene conservation in bacterial pangenomes.
Highlights
Regulation of gene expression is recognized as a key component in the cellular response to the environment
Using the model symbiont Sinorhizobium meliloti we have predicted the regulatory targets of 41 transcription factors in 51 strains and 5 other rhizobial species, showing a correlation between regulon diversity and pangenome evolution, through upstream sequence diversity and accessory genome composition
We have shown that genes not wired to the regulatory network are more likely to belong to the accessory genome, suggesting that inclusion in the regulatory circuits may be an indicator of gene conservation
Summary
Regulation of gene expression is recognized as a key component in the cellular response to the environment. This is especially true in the microbial world, for two reasons: bacterial cells are often under severe energy constraints, the most important being protein translation [1] and they usually face a vast range of environmental and physiological conditions; being able to efficiently and readily react to ever changing conditions can most certainly give a selective advantage over competitors and give rise to specific regulatory networks. Transcription is mainly regulated by proteins, called transcription factors (TF), which usually contain a protein domain capable of binding to specific DNA sequences, called TF binding sites (TFBS). Since TFBS can have variations around a preferred sequence, the affinity of a TF for its TFBSs covers a continuous range of values; since the TF binding strength appears to follow a sigmoid behaviour, it is possible to distinguish between ‘weak’ and ‘strong’ TFBSs [4]
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