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Published online on April 30, 2008
Proc. Natl. Acad. Sci. USA, 10.1073/pnas.0801269105


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MICROBIOLOGY
Host and invader impact of transfer of the clc genomic island into Pseudomonas aeruginosa PAO1

Muriel Gaillard*, Nataskha Pernet*, Christelle Vogne*, Otto Hagenbüchle{dagger},{ddagger}, and Jan Roelof van der Meer*,§

*Department of Fundamental Microbiology and {dagger}Centre of Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland; and {ddagger}Institute Suisse de Recherche Expérimentale sur le Cancer, 1066 Epalinges, Switzerland

Edited by Daniel L. Hartl, Harvard University, Cambridge, MA, and approved March 18, 2008 (received for review February 7, 2008)

Abstract

Genomic islands, large potentially mobile regions of bacterial chromosomes, are a major contributor to bacteria evolution. Here, we investigated the fitness cost and phenotypic differences between the bacterium Pseudomonas aeruginosa PAO1 and a derivative carrying one integrated copy of the clc element, a 103-kb genomic island [and integrative and conjugative element (ICE)] originating in Pseudomonas sp. strain B13 and a close relative of genomic islands found in clinical and environmental isolates of P. aeruginosa. By using a combination of whole genome transcriptome profiling, phenotypic arrays, competition experiments, and biofilm formation studies, only few differences became apparent, such as reduced biofilm growth and fourfold stationary phase repression of genes involved in acetoin metabolism in PAO1 containing the clc element. In contrast, PAO1 carrying the clc element acquired the capacity to grow on 3-chlorobenzoate and 2-aminophenol as sole carbon and energy substrates. No fitness loss >1% was detectable in competition experiments between PAO1 and PAO1 carrying the clc element. The genes from the clc element were not silent in PAO1, and excision was observed, although transfer of clc from PAO1 to other recipient bacteria was reduced by two orders of magnitude. Our results indicate that newly acquired mobile DNA not necessarily invoke an important fitness cost on their host. Absence of immediate detriment to the host may have contributed to the wide distribution of genomic islands like clc in bacterial genomes.

evolution | fitness | horizontal gene transfer


Footnotes

Author contributions: J.R.v.d.M. designed research; M.G., N.P., C.V., O.H., and J.R.v.d.M. performed research; M.G., N.P., O.H., and J.R.v.d.M. analyzed data; and M.G. and J.R.v.d.M. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

§To whom correspondence should be addressed. E-mail: janroelof.vandermeer{at}unil.ch

© 2008 by The National Academy of Sciences of the USA


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