Role of the virulence plasmid in acid resistance of Shigella flexneri

Chang Niu,Yong Cui,Xiaoqing Liu,Li Zhu,Jing Yang,Hongsheng Liu,Wei Xiao,Ruifeng Wang,Dongshu Wang,Hengliang Wang,Erling Feng,Huijie Xu,Chao Pan,Xiankai Liu

doi:10.1038/srep46465

Chang Niu, Yong Cui + Show 12 more

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https://doi.org/10.1038/srep46465

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Abstract

Virulence plasmid (VP) acquisition was a key step in the evolution of Shigella from a non-pathogenic Escherichia coli ancestor to a pathogenic genus. In addition, the co-evolution and co-ordination of chromosomes and VPs was also a very important step in the evolutionary process. To investigate the cross-talk between VPs and bacterial chromosomes, we analyzed the expression profiles of protein complexes and protein monomers in three wild-type Shigella flexneri strains and their corresponding VP deletion mutants. A non-pathogenic wild-type E. coli strain and mutant E. coli strains harboring three Shigella VPs were also analyzed. Comparisons showed that the expression of chromosome-encoded proteins GadA/B and AtpA/D, which are associated with intracellular proton flow and pH tuning of bacterial cells, was significantly altered following acquisition or deletion of the VP. The acid tolerance of the above strains was also compared, and the results confirmed that the presence of the VP reduced the bacterial survival rate in extremely acidic environments, such as that in the host stomach. These results further our understanding of the evolution from non-pathogenic E. coli to Shigella, and highlight the importance of co-ordination between heterologous genes and the host chromosome in the evolution of bacterial species.

Highlights

Virulence plasmid (VP) acquisition was a key step in the evolution of Shigella from a non-pathogenic Escherichia coli ancestor to a pathogenic genus
Shigella species and Escherichia coli have a high degree of homology at the genomic level, with the main difference lying in the presence of a 230-kb virulence plasmid (VP)
To examine the interactions between the VP and chromosomal genes, we deleted the VPs from several S. flexneri strains and introduced them into E. coli

Summary

Introduction

Virulence plasmid (VP) acquisition was a key step in the evolution of Shigella from a non-pathogenic Escherichia coli ancestor to a pathogenic genus. Whole-genome sequencing, including both VPs and chromosomes, has been completed for many strains of all four Shigella species[1,2] This large amount of genetic information allows us to identify the continuous genetic events that led to the evolution of pathogenic Shigella from non-pathogenic E. coli. Such regulatory hierarchy is relatively unstudied, with only one previous report in which a single VP-cured S. flexneri strain was analyzed[6] Regardless, this initial information suggests that the co-evolution and co-ordination of chromosomes and VPs are very important steps in the evolutionary process[7,8], and should be thoroughly analyzed for a more reliable and extensive understanding of the evolution of this pathogen. Three different S. flexneri strains were included in this study to gain a broader and more reliable understanding of the interaction between the VPs and the bacterial chromosomes

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