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Journal of Bacteriology, October 2009, p. 6003-6011, Vol. 191, No. 19
0021-9193/09/$08.00+0     doi:10.1128/JB.00687-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Identification of the Site-Specific DNA Invertase Responsible for the Phase Variation of SusC/SusD Family Outer Membrane Proteins in Bacteroides fragilis{triangledown} ,{dagger}

Haruyuki Nakayama-Imaohji,1 Hideki Hirakawa,2 Minoru Ichimura,1 Shin Wakimoto,1 Satoru Kuhara,3 Tetsuya Hayashi,4 and Tomomi Kuwahara1*

Department of Molecular Bacteriology, Institute of Health Biosciences, The University of Tokushima Graduate School, 3-18-15 Kuramoto-cho, Tokushima, 770-8503, Japan,1 Laboratory of Plant Genome Informatics, Department of Plant Genome Research, Kazusa DNA Research Institute, 2-6-7 Kazusakamatari, Kisarazu, Chiba, 292-0818, Japan,2 Department of Genetic Resources Technology, Faculty of Agriculture, Kyushu University, Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan,3 Frontier Science Research Center, University of Miyazaki, 5200 Kiyotake, Miyazaki 889-1692, Japan4

Received 26 May 2009/ Accepted 22 July 2009

The human gut microbe Bacteroides fragilis can alter the expression of its surface molecules, such as capsular polysaccharides and SusC/SusD family outer membrane proteins, through reversible DNA inversions. We demonstrate here that DNA inversions at 12 invertible regions, including three gene clusters for SusC/SusD family proteins, were controlled by a single tyrosine site-specific recombinase (Tsr0667) encoded by BF0667 in B. fragilis strain YCH46. Genetic disruption of BF0667 diminished or attenuated shufflon-type DNA inversions at all three susC/susD genes clusters, as well as simple DNA inversions at nine other loci, most of which colocalized with susC/susD family genes. The inverted repeat sequences found within the Tsr0667-regulated invertible regions shared the consensus motif sequence AGTYYYN4GDACT. Tsr0667 specifically mediated the DNA inversions of 10 of the 12 regions, even under an Escherichia coli background when the invertible regions were exposed to BF0667 in E. coli cells. Thus, Tsr0667 is an additional globally acting DNA invertase in B. fragilis, which probably involves the selective expression of SusC/SusD family outer membrane proteins.

* Corresponding author. Mailing address: Department of Molecular Bacteriology, Institute of Health Biosciences, The University of Tokushima Graduate School, 3-18-15 Kuramoto-cho, Tokushima 770-8503, Japan. Phone and fax: 81-88-633-9229. E-mail: tomomi{at}basic.med.tokushima-u.ac.jp

{triangledown} Published ahead of print on 31 July 2009.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, October 2009, p. 6003-6011, Vol. 191, No. 19
0021-9193/09/$08.00+0     doi:10.1128/JB.00687-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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