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Journal of Bacteriology, April 2007, p. 3091-3098, Vol. 189, No. 8
0021-9193/07/$08.00+0     doi:10.1128/JB.01906-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Region-Specific Insertion of Transposons in Combination with Selection for High Plasmid Transferability and Stability Accounts for the Structural Similarity of IncP-1 Plasmids{triangledown}

Masahiro Sota,1 Masataka Tsuda,2 Hirokazu Yano,2 Haruo Suzuki,1 Larry J. Forney,1 and Eva M. Top1*

Department of Biological Sciences, University of Idaho, Moscow, Idaho 83844-3051,1 Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Sendai 980-8577, Japan2

Received 18 December 2006/ Accepted 29 January 2007

The overall architecture of IncP-1 plasmids is very conserved in that the accessory genes are typically located in one or two specific regions: between oriV and trfA and between the tra and trb operons. Various hypotheses have been formulated to explain this, but none have been tested experimentally. We investigated whether this structural similarity is due to region-specific transposition alone or also is reliant on selection for plasmids with insertions limited to these two regions. We first examined the transposition of Tn21Km into IncP-1ß plasmid pBP136 and found that most Tn21Km insertions (67%) were located around oriV. A similar experiment using the oriV region of IncP-1ß plasmid pUO1 confirmed these results. We then tested the transferability, stability, and fitness cost of different pBP136 derivatives to determine if impairment of these key plasmid characters explained the conserved plasmid architecture. Most of the pBP136 derivatives with insertions in transfer genes were no longer transferable. The plasmids with insertions in the oriV-trfA and tra-trb regions were more stable than other plasmid variants, and one of these also showed a significantly lower fitness cost. In addition, our detailed sequence analysis of IncP-1 plasmids showed that Tn402/5053-like transposons are situated predominantly between the tra and trb operons and close to the putative resolution site for the ParA resolvase, a potential hot spot for those transposons. Our study presents the first empirical evidence that region-specific insertion of transposons in combination with selection for transferable and stable plasmids explains the structural similarity of IncP-1 plasmids.

* Corresponding author. Mailing address: University of Idaho, Department of Biological Sciences, P.O. Box 443051, Moscow, ID 83844-3051. Phone: (208) 885-5015. Fax: (208) 885-7905. E-mail: evatop{at}uidaho.edu

{triangledown} Published ahead of print on 2 February 2007.

Journal of Bacteriology, April 2007, p. 3091-3098, Vol. 189, No. 8
0021-9193/07/$08.00+0     doi:10.1128/JB.01906-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.





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