Transcriptomic analysis of the sulfate starvation response of Pseudomonas aeruginosa

Abstract

Pseudomonas aeruginosa is an opportunistic pathogen that causes a number of infections in humans, but is best known for its association with cystic fibrosis. It is able to use a wide range of sulfur compounds as sources of sulfur for growth. Gene expression in response to changes in sulfur supply was studied in P. aeruginosa E601, a cystic fibrosis isolate that displays mucin sulfatase activity, and in P. aeruginosa PAO1. A large family of genes was found to be upregulated by sulfate limitation in both isolates, encoding sulfatases and sulfonatases, transport systems, oxidative stress proteins, and a sulfate-regulated TonB/ExbBD complex. These genes were localized in five distinct islands on the genome and encoded proteins with a significantly reduced content of cysteine and methionine. Growth of P. aeruginosa E601 with mucin as the sulfur source led not only to a sulfate starvation response but also to induction of genes involved with type III secretion systems.

FIG. 1.

Functional classification of P. aeruginosa genes that displayed greater-than-twofold altered expression (P < 0.05) in the absence of sulfate compared to growth with sulfate as the sulfur source. The responses of P. aeruginosa PAO1 and P. aeruginosa E601 are shown separately. LPS, lipopolysaccharide.

FIG. 2.

(A) Sulfur content of sulfate starvation-regulated genes (see Table S2 in the supplemental material) in P. aeruginosa PAO1. (B) Distribution of SSI genes (see Table S3 in the supplemental material) on the P. aeruginosa genome, showing the presence of five islands that contain enhanced levels of sulfate starvation-regulated genes (sulfur islands I to V). (C) Distribution of genes encoding LSPs in the P. aeruginosa genome. The frequency is given as the number of LSP-encoding genes in a 10-gene window. LSPs were defined as proteins for which the percentage of encoded cysteine and methionine residues (not including fMet) was more than 1.5 standard deviations below the average value for all ORFs in the genome of 2.87%. The islands of SSI genes (I to V) (as described for panel B) are shown for comparison.