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


RESULTS
RGPs 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.


CONCLUSIONS
This 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.
Ogier
Jean-Claude
JC
INRA, UMR 1133, Laboratoire EMIP, Place Eugène Bataillon, F-34095 Montpellier, France.
Calteau
Alexandra
A
Forst
Steve
S
Goodrich-Blair
Heidi
H
Roche
David
D
Rouy
Zoé
Z
Suen
Garret
G
Zumbihl
Robert
R
Givaudan
Alain
A
Tailliez
Patrick
P
Médigue
Claudine
C
Gaudriault
Sophie
S
D000818:Animals; D002874:Chromosome Mapping; D002876:Chromosomes, Bacterial / Q000235:genetics; D019143:Evolution, Molecular; D005260:Female; D015321:Gene Rearrangement / Q000235:genetics; D005798:Genes, Bacterial / Q000235:genetics; D056426:Genetic Loci / Q000235:genetics; D014644:Genetic Variation; D016680:Genome, Bacterial / Q000235:genetics*; D023281:Genomics / Q000379:methods*; D054884:Host-Pathogen Interactions / Q000235:genetics*; D006801:Humans; D007448:Invertebrates / Q000382:microbiology*; D020637:Photorhabdus / Q000235:genetics*; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017384:Sequence Deletion / Q000235:genetics; D026801:Synteny / Q000235:genetics; D013997:Time Factors; D020593:Xenorhabdus / Q000235:genetics*
D012336:RNA, Ribosomal, 16S