Genome Plasticity and ori-ter Rebalancing in Salmonella typhi

Abstract

Genome plasticity resulting from frequent rearrangement of the bacterial genome is a fascinating but poorly understood phenomenon. First reported in Salmonella typhi, it has been observed only in a small number of Salmonella serovars, although the over 2,500 known Salmonella serovars are all very closely related. To gain insights into this phenomenon and elucidate its roles in bacterial evolution, especially those involved in the formation of particular pathogens, we systematically analyzed the genomes of 127 wild-type S. typhi strains isolated from many places of the world and compared them with the two sequenced strains, Ty2 and CT18, attempting to find possible associations between genome rearrangement and other significant genomic features. Like other host-adapted Salmonella serovars, S. typhi contained large genome insertions, including the 134 kb Salmonella pathogenicity island, SPI7. Our analyses showed that SPI7 disrupted the physical balance of the bacterial genome between the replication origin (ori) and terminus (ter) when this DNA segment was inserted into the genome, and rearrangement in individual strains further changed the genome balance status, with a general tendency toward a better balanced genome structure. In a given S. typhi strain, genome diversification occurred and resulted in different structures among cells in the culture. Under a stressed condition, bacterial cells with better balanced genome structures were selected to greatly increase in proportion; in such cases, bacteria with better balanced genomes formed larger colonies and grew with shorter generation times. Our results support the hypothesis that genome plasticity as a result of frequent rearrangement provides the opportunity for the bacterial genome to adopt a better balanced structure and thus eventually stabilizes the genome during evolution.

Fitness Effects of Replichore Imbalance in Salmonella enterica

“…A duplication that introduced a replichore imbalance of 23°did have a growth defect, but whether the defect is from replichore imbalance or the gene content of the duplication could not be distinguished. This study suggests that the disruption of replichore balance by acquisition of horizontally transferred genes is not the cause of chromosome rearrangements in host-specific S. enterica serovars as hypothesized (12)(13)(14).…”

Does Gene Translocation Accelerate the Evolution of Laterally Transferred Genes?

“…The host with translocated genes might be able to adapt to a new niche faster than if it depended solely on substitution. Indeed, it has been shown that large-scale genome rearrangements, such as gene inversion and gene translocation, alter gene expression (Brinig et al 2006) and might play roles in niche adaptation (Colson et al 2004;Kuwahara et al 2004;Burgetz et al 2006;Coleman et al 2006;Liu et al 2006).…”

Genome Rearrangements, Deletions, and Amplifications in the Natural Population of Bartonella henselae

“…Two hypotheses have previously been suggested to explain selection for locally high rearrangement frequencies. The adopt-adapt model suggests that the insertion of phages and/or GEIs leads to an unbalancing of the genome and thereby to fixation of chromosomal rearrangements, as observed in Salmonella enterica (46,47). According to the adoptadapt hypothesis, rearrangements occur until the chromosome is partitioned equally on both sides of ori and ter.…”