The SHI-3 iron transport island of Shigella boydii 0-1392 carries the genes for aerobactin synthesis and transport

Abstract

In Shigella boydii 0-1392, genes encoding the synthesis and transport of the hydroxamate siderophore aerobactin are located within a 21-kb iron transport island between lysU and the pheU tRNA gene. DNA sequence analysis of the S. boydii 0-1392 island, designated SHI-3 for Shigella island 3, revealed a conserved aerobactin operon associated with a P4 prophage-like integrase gene and numerous insertion sequences (IS). SHI-3 is present at the pheU tRNA locus in some S. boydii isolates but not in others. The map locations of the aerobactin genes vary among closely related species. The association of the aerobactin operon with phage genes and mobile elements and its presence at different locations within the genomes of enteric pathogens suggest that these virulence-enhancing genes may have been acquired by bacteriophage integration or IS element-mediated transposition. An S. boydii aerobactin synthesis mutant, 0-1392 iucB, was constructed and was similar to the wild type in tissue culture assays of invasion and intercellular spread.

FIG. 1

Map of the S. boydii 0-1392 aerobactin island, SHI-3, and the corresponding E. coli K-12 region between pheU and lysU at min 94. Sequences present in both E. coli K-12 and S. boydii are indicated by the black bars and are designated K-12 on the SHI-3 map. The ORFs, indicated as shiB and o2 to o4, were inferred from sequence analysis. The iucA probe and the int3 probe, as well as the approximate positions of primers used for PCR amplification of the junctions, are positioned below the SHI-3 map.

FIG. 2

The P4-like integrase and aerobactin genes are linked in several S. boydii serotypes. Genomic DNA was digested with PvuII, and the fragments were hybridized to a 1-kb iucA probe or a 395-bp int3 probe. Locations of the probes are shown in Fig. 1. Lane 1, S. boydii 0-1392; lane 2, S. boydii 0-1393; lane 3, S. boydii 224860.

FIG. 3

Map locations of the aerobactin genes among the Enterobacteriaceae. The islands containing aerobactin genes are shown as insertions relative to the E. coli K-12 chromosome. Hatched boxes indicate the aerobactin operon, white boxes indicate P4-like prophage integrase genes, and dark grey boxes indicate ISs. (a) The SHI-2 aerobactin pathogenicity island at selC in some S. flexneri strains and in S. sonnei. (b) The SHI-3 aerobactin island at pheU in S. boydii. (c) The aerobactin genes are encoded on the pColV and F1me plasmids in some strains of E. coli and Salmonella enterica, respectively. On pColV, the aerobactin genes are flanked by IS1 elements.