Genomic evolution of Vibrio cholerae

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Vibrio cholera, the causal agent of cholera, also occupies an autochthonous aquatic inhabitant. The current, seventh cholera pandemic is linked to O1 El Tor biotype and O139 serogroups. In the last decades, we have witnessed a shift involving genetically and phenotypically varied pandemic clones in Asia and Africa. Recent comparative genomic studies have identified a large ‘mobilome’, or composed of mobile genomic islands in V. cholerae. All seventh pandemic isolates have highly related genome sequences, but they can be differentiated by set of these genomic islands. A consequence of the extensive lateral gene transfer is that classically important diagnostic markers, such as serotype and biotype, are not reliable and new methods based on genomic sequences are required.

Introduction

Cholera, an acute life-threatening diarrheal disease, is caused by the bacterium, Vibrio cholerae that is also an autochthonous aquatic inhabitant. Even though the incidences of cholera were recorded in ancient India and China, the modern history of cholera began in 1817, when the first pandemic started in India [1]. So far, seven cholera pandemics are recognized but actual bacterial isolates are only available for the sixth (1899–1923) and seventh (1961–present) pandemics.

V. cholerae, the type species of the genus Vibrio, can be further classified into different serogroups determined by the structure of the O antigen in lipopolysaccharide (LPS). While over 200 serogroups have been recognized to date, only the O1 and O139 serogroups have been linked to epidemic and pandemic cholera in humans. The O1 serogroup is further classified into two biotypes, namely classical and El Tor, by differences in phenotypic traits such as biochemical reactions and susceptibility to specific bacteriophages [2, 3]. Epidemic V. cholerae strains harbour cholera toxin (CT), encoded by two genes (ctxAB) and other key virulence factors in their mobile genetic element repertoire [4].

It is well documented that isolates of the sixth pandemic were almost exclusively of the V. cholerae O1 classical biotype whereas the current seventh pandemic has been caused by the O1 El Tor biotypes, first isolated on the Indonesian island of Sulawesi in 1961 [5]. Since then, several novel genetic variants of V. cholerae O1 El Tor have emerged or re-emerged. Most notable was a new serogroup of the species, named O139 or Bengal. This serogroup, first recognized in 1992 in India and Bangladesh, initially displaced the local existing O1 El Tor strains [6], though it is now restricted to Asia. The current pandemic in Asia and Africa is currently largely attributed to new variants of V. cholerae showing traits of both the classical and El Tor biotypes and El Tor biotype strains producing the classical cholera toxin. Safa et al. [7••] coined the term, ‘atypical El Tor’, for these clones, which include the Matlab types I, II, and III [8], altered El Tor [9], Mozambique El Tor [10, 11] and hybrid El Tor strains [12].

In recent years, several studies were carried out to elucidate the evolutionary nature and mechanism of these clonal shifts among genetically distinctive V. cholerae isolates using comparative genomics [13, 14, 15••, 16•]. Here, we will focus on genomic evolution of V. cholerae in light of genome wide comparison of available whole genome sequence data.

Section snippets

Genome-based phylogeny of V. cholerae and related taxa

To date, more than 60 complete or draft whole genome sequences are available in the public domain for various Vibrio species, including over 26 V. cholerae strains. Among Vibrio spp., Vibrio mimicus was thought to be genetically related to V. cholerae [17], as it was originally reported to be a biochemically atypical group of V. cholerae strains [18]. A clearer appraisal of the relationship emerged from the genome-based phylogenetic analysis (Figure 1), where both V. cholerae and V. mimicus

Serogroups, biotypes and genotypes of V. cholerae

From the dawn of bacteriology, serotyping and biotyping have played a crucial role in diagnostics and epidemiology of V. cholerae. Therefore, the emergence of a new serogroup, O139, in the midst of the seventh pandemic was a huge surprise to microbiologists and clinicians [20, 21]. Soon after its discovery, multiple studies suggested that the O139 clones originated from O1 El Tor progenitor(s) with the laterally transferred O139 antigen encoding genomic island [22, 23], rather than from non-O1

The mobilome of V. cholerae

The mobilome is the total of all mobile genetic elements in a genome, and perhaps a large mobilome is a characteristic of prokaryotic species [25]. Chun et al. [15••] employed a multi-way comparative genomics approach to define the first mobilome database of V. cholerae, comprising 73 newly identified genomic islands in addition to known mobile elements such as Vibrio Pathogenicity Island (VPI) [26] and CTX-prophage [4]. Advantages of this approach over conventional computational methods for

Genesis of the seventh pandemic V. cholerae

Whole genome-based comparisons of representative V. cholerae strains belonging to various serogroups and genomically distinctive lineages indicated that isolates responsible for the seventh pandemic are clonal, despite belonging to either O1 or O139 serotypes [15••]. All of the seventh pandemic V. cholerae strains sequenced so far share an almost identical genome backbone, whereas most variation lies in their gene contents. Within the PG-1 group (Figure 2), a major difference between O1 El Tor

Future perspectives

Even though V. cholerae is one of the bacterial species with the most representative genome sequences in the public domain, more work is needed to reveal the fine details of the evolutionary mechanism behind the emergence of the seventh pandemic clones. Fortunately, next generation sequencing technologies allowing affordable genome sequencing, can facilitate large-scale population genetics studies. Overall evolutionary networks among closely related seventh pandemic strains could be unraveled

Conclusions

Due to the invention of next generation sequencing technology, large-scale comparative genomics has become feasible for important bacterial human pathogens, such as Salmonella typhi [30], Bacillus anthracis [31] and Escherichia coli/Shigella [32, 33]. Unlike these species, V. cholerae is a true inhabitant of the environment, a non-clonal species, and is the cause of pandemics and thereby offers a prime example and framework to explain the general mechanism of the short-term and long-term

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgment

This work was supported by the National Research Foundation of Korea (NRF) grant (#0427-20100006) funded by the Korea government (MEST).

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