Core-genome scaffold comparison reveals the prevalence that inversion events are associated with pairs of inverted repeats

Abstract

Background: Genome rearrangement describes gross changes of chromosomal regions, plays an important role in evolutionary biology and has profound impacts on phenotype in organisms ranging from microbes to humans. With more and more complete genomes accomplished, lots of genomic comparisons have been conducted in order to find genome rearrangements and the mechanisms which underlie the rearrangement events. In our opinion, genomic comparison of different individuals/strains within the same species (pan-genome) is more helpful to reveal the mechanisms for genome rearrangements since genomes of the same species are much closer to each other.

Results: We study the mechanism for inversion events via core-genome scaffold comparison of different strains within the same species. We focus on two kinds of bacteria, Pseudomonas aeruginosa and Escherichia coli, and investigate the inversion events among different strains of the same species. We find an interesting phenomenon that long (larger than 10,000 bp) inversion regions are flanked by a pair of Inverted Repeats (IRs). This mechanism can also explain why the breakpoint reuses for inversion events happen. We study the prevalence of the phenomenon and find that it is a major mechanism for inversions. The other observation is that for different rearrangement events such as transposition and inverted block interchange, the two ends of the swapped regions are also associated with repeats so that after the rearrangement operations the two ends of the swapped regions remain unchanged. To our knowledge, this is the first time such a phenomenon is reported for transposition event.

Conclusions: In both Pseudomonas aeruginosa and Escherichia coli strains, IRs were found at the two ends of long sequence inversions. The two ends of the inversion remained unchanged before and after the inversion event. The existence of IRs can explain the breakpoint reuse phenomenon. We also observed that other rearrangement operations such as transposition, inverted transposition, and inverted block interchange, had repeats (not necessarily inverted) at the ends of each segment, where the ends remained unchanged before and after the rearrangement operations. This suggests that the conservation of ends could possibly be a popular phenomenon in many types of chromosome rearrangement events.

Keywords: Comparative genomics; Genome rearrangment; Inversion; Inverted block interchange; Transposition.

Fig. 1

The breakpoint graph for an independent transposition

Fig. 2

The breakpoint graph for an independent block interchange

Fig. 3

Eight groups of scaffolds for the 25 Pseudomonas aeruginosa strains. Each orange block stands for a merged block which may represent several consecutive core-genome blocks. The numbers above each orange block indicate the included core-genome blocks, for example, 1$\backsim$5 means the orange block includes five core-genome blocks, which are Blocks 1, 2, 3, 4 and 5. Repeats A, B, O and R are represented by blue, red, purple and green triangles respectively. The arrow directions indicate positive/negative strand

Fig. 4

Three inversion steps from scaffold 1 to scaffold 5. The breakpoint between -6 and 64 in Scaffold 5 is used three times. See the black arrow

Fig. 5

The role of repeats in transposition event. Both Scaffolds 1 and 7 contain four merged core blocks (1$\backsim$17), (18$\backsim$46), (47$\backsim$60), and (61$\backsim$69). Moreover, both Scaffolds 1 and 7 contain another two non-core blocks DS1 and DS2, where the occurrences of DS1 and DS2 in both scaffolds are 100% identical. There are three occurrences of a repeat +R in both scaffolds

Fig. 6

Nine groups of scaffolds for the 31 Escherichia coli strains

Fig. 7

Three inversions between Scaffolds 1 and 7. The breakpoint between 41 and 42 in Scaffold 1 is used twice. See the black arrow

Fig. 8

Inverted block interchange of Region -27$\backsim$-20 and Region -13$\backsim$-11 between Scaffolds 6 and 1. +E/-E and +S/-S are two pairs of IRs. The steps from Scaffold 6 to the middle scaffold are omitted

Fig. 9

Two inversions which can replace the inverted block interchange of Regions -27$\backsim$-20 and -13$\backsim$-11 between Scaffold 6 and 1. The first inversion is flanked by +E and -E and the second inversion is flanked by +S and -S. The steps from the Scaffold 6 to its next scaffold are omitted

Fig. 10

Inverted transposition of Region 16$\backsim$19 and Block 15 between Scaffold 9 and 1. There are three occurrences of Repeat Q with different signs. From Scaffold 9 to the next scaffold, there is an inversion of Block 48 which are flanked by +F and -F

Fig. 11

Two inversions which can replace the inverted transposition of Region 16$\backsim$19 and Block 15 between Scaffold 9 and 1. Both of the two inversions are flanked by a pair of IRs (+Q/-Q). From Scaffold 9 to the next scaffold, there is an inversion of Block 48 which are flanked by +F and -F