Dynamics of Pseudomonas aeruginosa genome evolution

*Department of Molecular Microbiology and Immunology, College of Medicine,
^†Department of Biological Sciences, College of Arts and Sciences, and
^‡Bioinformatics Research Group (BioRG), School of Computing and Information Sciences, College of Engineering, Florida International University, Miami, FL 33199;
^§Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, MA 02115; and
^¶The Broad Institute of MIT and Harvard, Cambridge, MA 02142

Communicated by John J. Mekalanos, Harvard Medical School, Boston, MA, December 19, 2007 (received for review November 21, 2007)

Abstract

One of the hallmarks of the Gram-negative bacterium Pseudomonas aeruginosa is its ability to thrive in diverse environments that includes humans with a variety of debilitating diseases or immune deficiencies. Here we report the complete sequence and comparative analysis of the genomes of two representative P. aeruginosa strains isolated from cystic fibrosis (CF) patients whose genetic disorder predisposes them to infections by this pathogen. The comparison of the genomes of the two CF strains with those of other P. aeruginosa presents a picture of a mosaic genome, consisting of a conserved core component, interrupted in each strain by combinations of specific blocks of genes. These strain-specific segments of the genome are found in limited chromosomal locations, referred to as regions of genomic plasticity. The ability of P. aeruginosa to shape its genomic composition to favor survival in the widest range of environmental reservoirs, with corresponding enhancement of its metabolic capacity is supported by the identification of a genomic island in one of the sequenced CF isolates, encoding enzymes capable of degrading terpenoids produced by trees. This work suggests that niche adaptation is a major evolutionary force influencing the composition of bacterial genomes. Unlike genome reduction seen in host-adapted bacterial pathogens, the genetic capacity of P. aeruginosa is determined by the ability of individual strains to acquire or discard genomic segments, giving rise to strains with customized genomic repertoires. Consequently, this organism can survive in a wide range of environmental reservoirs that can serve as sources of the infecting organisms.

Footnotes

**To whom correspondence should be addressed. E-mail: stephen_lory{at}hms.harvard.edu
Author contributions: K.M., G.N., C.V., X.Q., J.M.M., M.K., A.R., C.N.Y., R.E., E.Z., R.O., M.D., P.M., J.R.W., P.A.G., C.K., B.B., J.E.G., and S.L. designed research; G.N., X.Q., J.M.M., A.R., R.E., R.O., M.D., R.S.S., P.M., J.R.W., and P.A.G. performed research; K.M., G.N., C.V., X.Q., M.K., A.R., C.N.Y., R.E., E.Z., R.S.S., P.M., J.R.W., P.A.G., C.K., J.E.G., and S.L. analyzed data; and K.M., G.N., M.K., P.A.G., C.K., and S.L. wrote the paper.
↵ ^‖Present address: Department of Biological Sciences, Vanderbilt University, VU Station B 351634, Nashville, TN 37235.
The authors declare no conflict of interest.
Data deposition: The data reported in this paper have been deposted in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo [accession nos. NZ_AAKW00000000 (PA2192) and NZ_AAKV00000000 (C3719)].
This article contains supporting information online at www.pnas.org/cgi/content/full/0711982105/DC1.
Freely available online through the PNAS open access option.