Evolution of Intra-specific Regulatory Networks in a Multipartite Bacterial Genome

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.

The Divided Bacterial Genome: Structure, Function, and Evolution

“…An in silico regulon analysis predicted that most S. meliloti transcriptional factors regulate genes on the same replicon (147). However, a subset was predicted to regulate genes across multiple replicons, and there was a bias for chromosomal regulators to modulate chromid/megaplasmid genes compared to the number of chromid/megaplasmid regulators predicted to regulate chromosomal genes (147). Consistent with this, the cell cycle regulator CtrA and the symbiotic nitrogen fixation regulator FixJ regulate genes on all three replicons in S. meliloti while preferentially regulating genes on the same replicon that they are encoded on (148,149).…”

Bacterial Biosensors for in Vivo Spatiotemporal Mapping of Root Secretion

“…As these biosensors are plasmid based, it is possible to transfer them into different bacterial backgrounds (e.g. mutant strains of R. leguminosarum or other species of bacteria), although their expression in heterologous hosts may be limited by regulatory elements (Galardini et al, 2015). Each of the 14 lux reporters was tested on 26 different sugars and polyols and/or on a set of 18 selected compounds (organic acids, amino acids, and plant metabolites) to establish the specificity of the induction of lux expression from each of the bioreporters (Table I; Supplemental Table S2).…”

Identification of Modules With Similar Gene Regulation and Metabolic Functions Based on Co-expression Data

“…Based on this approach, we identified that S. meliloti 1021 (Sme) is a module that contains a high proportion of orthologs with the other modules, where genes related to cellular metabolic process, primary metabolic process, nitrogen compound metabolic process and organism substance metabolic process were identified. This result could be associated to the prevalence of genetic redundancy in this bacterium, an in particular to those genes involved in a variety of metabolic pathways, including central carbon metabolism, transport, and amino acid biosynthesis (diCenzo and Finan, 2015); and the number of genes with some regulatory mechanisms identified in one of the three replicons, and the function of regulated genes was found to be in accordance with the overall replicon functional signature: housekeeping functions for the chromosome, metabolism for the chromid, and symbiosis for the megaplasmid (Galardini et al, 2015).…”