Molecular phylogeny of the salmonellae: relationships among Salmonella species and subspecies determined from four housekeeping genes and evidence of lateral gene transfer events

Abstract

The salmonellae are a diverse group of bacteria within the family Enterobacteriaceae that includes two species, Salmonella enterica and Salmonella bongori. In order to characterize the phylogenetic relationships of the species and subspecies of Salmonella, we analyzed four housekeeping genes, gapA, phoP, mdh and recA, comprising 3,459 bp of nucleotide sequence data for each isolate sequenced. Sixty-one isolates representing the most common serotypes of the seven subspecies of Salmonella enterica and six isolates of Salmonella bongori were included in this study. We present a robust phylogeny of the Salmonella species and subspecies that clearly defines the lineages comprising diphasic and monophasic subspecies. Evidence of intersubspecies lateral gene transfer of the housekeeping gene recA, which has not previously been reported, was obtained.

FIG. 1.

Summary of previous phylogenetic studies. (a) Tree based on MLEE data from Boyd et al. (2). (b) Tree based on housekeeping gene sequence from Boyd et al. (2). (c) Tree based on gene acquisition data from microarray analysis from Porwollik et al. (26). (d) Tree based on invasion gene sequence from Boyd et al. (2).

FIG. 2.

Phylogeny based on individual gene sequences. Bayesian consensus of 900 trees from the individual nucleotide sequences. Support values of all major nodes are listed; internal branches with values higher than 0.75 are reported. Bars, 0.1 substitutions per site.

FIG. 3.

Phylogeny based on concatenated gene trees. Bayesian consensus of 900 trees representing the phylogeny of Salmonella based on the four housekeeping genes, recA, mdh, phoP, and gapA. The node support value represented by an asterisk denotes the weakly supported node prior to removal of the subspecies IIIa recA sequence.

FIG. 4.

(a) Representation of topology tests based on Bayesian consensus and best trees for recA and mdh. Swap refers to branch relocation to concatenated tree location for topology test. Control indicates branch relocation of S. bongori to subsp. I branch. (b) Statistical analyses of Bayesian trees testing the hypothesis of a recA and mdh LGT event. Cons, consensus tree; best, best tree; swap, tree with relocation of branch based on concatenated tree; control, tree relocation of Salmonella bongori branch to subsp. I.

FIG. 5.

Neighbor-joining tree generated from the average subspecies distance matrix. Dates labeled on each node are represented in millions of years ago.