Homologous recombination between rrn operons rearranges the chromosome in host-specialized species of Salmonella

Abstract

Partial digestion with I-CeuI, which digests bacterial DNA at the gene coding for the large subunit rRNA, established the rrn genomic skeleton (the distance in kb between rRNA operons) in 56 strains of Salmonella, from Salmonella Reference B (SARB) set. All had seven I-CeuI sites, indicating seven rrn operons. The order of I-CeuI fragments was ABCDEFG in S. typhimurium LT2 and in 31 other species, mostly host-generalists; in S. typhi, S. paratyphi C, S. gallinarum, and S. pullorum (host-specialized species), these fragments are rearranged, due to homologous recombination between the rrn operons. Rearrangements, such as inversions and translocations not involving the rrn operons, are rare. I-CeuI fragments of some species are larger than the norm, suggesting the insertion of unique blocks of DNA by lateral transfer from other species. z

The Evolving Genome of Salmonella enterica Serovar Pullorum

“…The previously mapped S. enterica serovar Pullorum strains had other genome structures that were not found here, with RKS2266 being ABDCFEG and RKS2246 being ABEDCFG (28). Most cleavage fragments with XbaI, AvrII, or SpeI were identical in size among all 16 strains, indicating that they were a tight phylogenetic group of bacteria (i.e., they were all "S. enterica serovar Pullorum"), though with significant variations in size of a small number of cleavage fragments, presumably a result of different genomic inversions or translocations in different strains.…”

“…S. enterica serovar Pullorum strains RKS5078, maintained at the Salmonella Genetic Stock Center (SGSC, www.ucalgary.ca/Ϸkesander) as SGSC2294, and RKS2242 (SGSC2295) were obtained from R. K. Selander, and strains 490 (SGSC2737), 498 (SGSC2738), 499 (SGSC2739), 501 (SGSC2740), 504 (SGSC2741), 505 (SGSC2742), 507 (SGSC2743), 509 (SGSC2745), 510 (SGSC2746), 512 (SGSC2747), 513 (SGSC2748), 514 (SGSC2749), 515 (SGSC2750), and R278 (SGSC2751) were obtained from C. Poppe. Previously, we have made I-CeuI maps on two S. enterica serovar Pullorum strains, RKS2266 (SGSC2508) and RKS2246 (SGSC2509) (28), so these two strains were not included in this study. RKS2266 and RKS2246, however, will be compared with RKS5078 in this study.…”

Host Specificity of Bacterial Pathogens

“…This might explain why major genomic rearrangements owing to homologous recombination between the rrn operons are a characteristic feature of the chromosomes of S. Typhi isolates Sanderson 1995, 1996;Kothapalli et al 2005;Matthews et al 2010). Similar genome rearrangements are also found in other host-restricted lineages within the genus Salmonella, including S. Paratyphi C, S. Gallinarum, and S. Typhimurium phage type DT2 (Liu and Sanderson 1998;Helm et al 2004;Wu et al 2005;Liu et al 2007). Thus, rearrangements are a genomic signature of host-restricted members of the genus Salmonella that rely on chronic persistence in the host for transmission.…”

Does Gene Translocation Accelerate the Evolution of Laterally Transferred Genes?

“…Gene translocations tend to take place in recently transferred genes that tend to be deleted rapidly; as a consequence, gene translocation should be considered as a local phenomenon. Indeed, relatively high rates of gene rearrangements have been found in closely related Salmonella strains (Liu and Sanderson 1998;Liu et al 2003;Kothapalli et al 2005), whereas the genome structures between Escherichia coli and Salmonella remain highly similar (Krawiec and Riley 1990;Liu et al 1993). Furthermore, most truncated genes were found in translocated genes and the proportion of truncated genes is much higher in translocated genes than in positionally conserved genes ( Figure 5).…”