Units of plasticity in bacterial genomes: new insight from the comparative genomics of two bacteria interacting with invertebrates, Photorhabdus and Xenorhabdus

Abstract

BackgroundFlexible genomes facilitate bacterial evolution and are classically organized into polymorphic strain-specific segments called regions of genomic plasticity (RGPs). Using a new web tool, RGPFinder, we investigated plasticity units in bacterial genomes, by exhaustive description of the RGPs in two Photorhabdus and two Xenorhabdus strains, belonging to the Enterobacteriaceae and interacting with invertebrates (insects and nematodes).ResultsRGPs account for about 60% of the genome in each of the four genomes studied. We classified RGPs into genomic islands (GIs), prophages and two new classes of RGP without the features of classical mobile genetic elements (MGEs) but harboring genes encoding enzymes catalyzing DNA recombination (RGPmob), or with no remarkable feature (RGPnone). These new classes accounted for most of the RGPs and are probably hypervariable regions, ancient MGEs with degraded mobilization machinery or non canonical MGEs for which the mobility mechanism has yet to be described. We provide evidence that not only the GIs and the prophages, but also RGPmob and RGPnone, have a mosaic structure consisting of modules. A module is a block of genes, 0.5 to 60 kb in length, displaying a conserved genomic organization among the different Enterobacteriaceae. Modules are functional units involved in host/environment interactions (22-31%), metabolism (22-27%), intracellular or intercellular DNA mobility (13-30%), drug resistance (4-5%) and antibiotic synthesis (3-6%). Finally, in silico comparisons and PCR multiplex analysis indicated that these modules served as plasticity units within the bacterial genome during genome speciation and as deletion units in clonal variants of Photorhabdus.ConclusionsThis led us to consider the modules, rather than the entire RGP, as the true unit of plasticity in bacterial genomes, during both short-term and long-term genome evolution.

Impact of Small Repeat Sequences on Bacterial Genome Evolution

“…These MITEs are also found in Xenorhabdus (Ogier et al 2010). Both Photorhabdus and Xenorhabdus belong to the Enterobacteriaceae family but are insect pathogens.…”

The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes

“…We also performed a detailed proteomic analysis of secreted proteins in X. nematophila , which we describe in Text S7, and note that a detailed analysis of regions of genome plasticity was performed previously for these two bacteria [60].…”

FliZ Is a Global Regulatory Protein Affecting the Expression of Flagellar and Virulence Genes in Individual Xenorhabdus nematophila Bacterial Cells

“…Many other non-flagellar functional clusters were also upregulated by FliZ (i) the 14 genes ( xcnA–N ; locus 15) required for the synthesis of xenocoumacin, the major antimicrobial compound produced by X. nematophila [31]; (ii) the pax cluster (locus 10) encoding enzymes involved in synthesis of the Pax antimicrobial cyclolipopeptide [32], [33] and (iii) all 16 genes (locus 23) encoding putative components of a type VI secretion system [34], [35]. Non-flagellar genes directly regulated by FliZ, such as those encoding hemolysins (XaxAB and XhlAB) [13], were identified, as expected.…”