Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis

Abstract

The presence of homologues of Salmonella enterica sv. Typhimurium LT2 genes was assessed in 22 other Salmonella including members of all seven subspecies and Salmonella bongori. Genomes were hybridized to a microarray of over 97% of the 4,596 annotated ORFs in the LT2 genome. A phylogenetic tree based on homologue content, relative to LT2, was largely concordant with previous studies using sequence information from several loci. Based on the topology of this tree, homologues of genes in LT2 acquired by various clades were predicted including 513 homologues acquired by the ancestor of all Salmonella, 111 acquired by S. enterica, 105 by diphasic Salmonella, and 216 by subspecies 1, most of which are of unknown function. Because this subspecies is responsible for almost all Salmonella infections of mammals and birds, these genes will be of particular interest for further mechanistic studies. Overall, a high level of gene gain, loss, or rapid divergence was predicted along all lineages. For example, at least 425 close homologues of LT2 genes may have been laterally transferred into Salmonella and then between Salmonella lineages.

Figure 1

Presence and absence of STM LT2 protein coding sequence homologues in 26 other enterobacterial strains including representatives of all Salmonella ssp and S. bongori (SBO). The numbers on top correspond to strain numbers in Table 1, column 6. Strains are sorted from left to right with ascending relatedness to LT2. The gene status is color-coded: blue, present; purple, uncertain; red, absent. For cutoffs of absence and presence predictions, refer to Materials and Methods. Some prominent regions are indicated. (A) The genes on the chromosome are represented in order of position in LT2 from STM 0001 to 4600. (B) The genes of the LT2 virulence plasmid pSLT.

Figure 2

Phylogenetic tree of the Salmonella clade. The cladogram was constructed with PAUP* software (Sinauer) by using maximum parsimony, equal weight, and 1,000 bootstraps with Y. pestis as the outgroup. Five crucial stages in Salmonella evolution are indicated: 1, divergence of Salmonella from E. coli; 2, separation of S. enterica from S. bongori; 3, evolution of the diphasic S. enterica strains; 4, partition of S. enterica ssp. I; and 5, development of STM. The number of genes predicted to be recruited at each node is shown in Table 3.