Comparative genomics of the family Vibrionaceae reveals the wide distribution of genes encoding virulence-associated proteins

Abstract

Background: Species of the family Vibrionaceae are ubiquitous in marine environments. Several of these species are important pathogens of humans and marine species. Evidence indicates that genetic exchange plays an important role in the emergence of new pathogenic strains within this family. Data from the sequenced genomes of strains in this family could show how the genes encoded by all these strains, known as the pangenome, are distributed. Information about the core, accessory and panproteome of this family can show how, for example, genes encoding virulence-associated proteins are distributed and help us understand how virulence emerges.

Results: We deduced the complete set of orthologs for eleven strains from this family. The core proteome consists of 1,882 orthologous groups, which is 28% of the 6,629 orthologous groups in this family. There were 4,411 accessory orthologous groups (i.e., proteins that occurred in from 2 to 10 proteomes) and 5,584 unique proteins (encoded once on only one of the eleven genomes). Proteins that have been associated with virulence in V. cholerae were widely distributed across the eleven genomes, but the majority was found only on the genomes of the two V. cholerae strains examined.

Conclusions: The proteomes are reflective of the differing evolutionary trajectories followed by different strains to similar phenotypes. The composition of the proteomes supports the notion that genetic exchange among species of the Vibrionaceae is widespread and that this exchange aids these species in adapting to their environments.

Figure 1

Frequency distribution of orthologous groups in the eleven genomes examined. The grey bars represent orthologous groups, while the white bar represents strain-unique proteins. 1,882 of the 6,629 orthologous groups are found in each of the 11 genomes. Only 336 of the orthologous groups are found in individual genomes. In addition to the orthologous groups, the pangenome contains 5,584 proteins that occur only once in one of the genomes.

Figure 2

Distribution of the 6,629 orthologous groups into COG functional categories. The number of orthologous groups in each COG category is represented by the bar height. The proportion of each COG category that is composed of core (black) or accessory (grey) orthologous groups is shown. Categories are arranged within each class in order of size. In most categories, at least half the orthologs are found in the core proteome, but COG category T (Signal transduction mechanisms) is overrepresented in the accessory proteome.

Figure 3

Heatmap of core and accessory orthologs found in V. cholerae N16961 and their distribution among the sequenced Vibrionaceae strains. The large (top) and small (bottom) chromosomes of the 11 strains are represented. Vertical blue or yellow bars represent the presence or absence, respectively, of each orthologous group in each genome. Vertical black bars represent proteins that are unique to V. cholerae N16961. The orthologous groups are arranged according to the encoding gene order on the V. cholerae N16961 chromosomes. Previously characterized genomic islands and the superintegron region are highlighted. The genomes are ordered top to bottom according to their phylogenetic relationships as shown in the dendrogram on the left. The dendrogram was calculated using the dollop algorithm from PHYLIP (see Methods) and is based on the presence or absence of the accessory orthologous groups.

Figure 4

Distribution of virulence-associated orthologous groups across eleven Vibrionaceae genomes. The presentation is as in Figure 3, except the dendrogram is eliminated to save space and virulence-associated proteins (both unique and orthologous) are shown as vertical red bars. In addition to the well-known genomic islands, three regions (A, B, and C) that were identified in this study and are discussed in the text are shown, along with the Che Cluster II and III regions. These regions are marked Che II and Che III respectively. Che Cluster I is within region C.