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Journal of Bacteriology, July 2009, p. 4111-4121, Vol. 191, No. 13
0021-9193/09/$08.00+0 doi:10.1128/JB.00251-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
Occurrence, Plasticity, and Evolution of the vpma Gene Family, a Genetic System Devoted to High-Frequency Surface Variation in Mycoplasma agalactiae
,
Laurent-Xavier Nouvel,1,2
Marc Marenda,1,2,
Pascal Sirand-Pugnet,3,4
Eveline Sagné,1,2
Michelle Glew,1,2,
Sophie Mangenot,5
Valérie Barbe,5
Aurélien Barré,6
Stéphane Claverol,7 and
Christine Citti1,2*
Université de Toulouse, ENVT, UMR 1225, F-31076 Toulouse, France,1 INRA, UMR 1225, F-31076 Toulouse, France,2 Université de Bordeaux, UB2, UMR1090, F-33076 Bordeaux, France,3 INRA, UMR 1090, F-33883 Villenave d'Ornon, France,4 CEA-IG, Genoscope, F-91057 Evry Cedex, France,5 Centre de Bioinformatique de Bordeaux, UB2, F-33076 Bordeaux, France,6 Pole Protéomique, Plateforme Génomique Fonctionnelle Bordeaux, UB2, 33076 Bordeaux, France7
Received 25 February 2009/ Accepted 10 April 2009
Mycoplasma agalactiae, an important pathogen of small ruminants, exhibits a very versatile surface architecture by switching multiple, related lipoproteins (Vpmas) on and off. In the type strain, PG2, Vpma phase variation is generated by a cluster of six vpma genes that undergo frequent DNA rearrangements via site-specific recombination. To further comprehend the degree of diversity that can be generated at the M. agalactiae surface, the vpma gene repertoire of a field strain, 5632, was analyzed and shown to contain an extended repertoire of 23 vpma genes distributed between two loci located 250 kbp apart. Loci I and II include 16 and 7 vpma genes, respectively, with all vpma genes of locus II being duplicated at locus I. Several Vpmas displayed a chimeric structure suggestive of homologous recombination, and a global proteomic analysis further indicated that at least 13 of the 16 Vpmas can be expressed by the 5632 strain. Because a single promoter is present in each vpma locus, concomitant Vpma expression can occur in a strain with duplicated loci. Consequently, the number of possible surface combinations is much higher for strain 5632 than for the type strain. Finally, our data suggested that insertion sequences are likely to be involved in 5632 vpma locus duplication at a remote chromosomal position. The role of such mobile genetic elements in chromosomal shuffling of genes encoding major surface components may have important evolutionary and epidemiological consequences for pathogens, such as mycoplasmas, that have a reduced genome and no cell wall.
* Corresponding author. Mailing address: UMR 1225 INRA, ENVT, Ecole Nationale Vétérinaire de Toulouse, 23 Chemin des Capelles, BP 87614, 31076 Toulouse Cedex 3, France. Phone: 33.(0)5.61.19.38.56. Fax: 33.(0)5.61.19.32.73. E-mail: c.citti{at}envt.fr
Published ahead of print on 17 April 2009.
Supplemental material for this article may be found at http://jb.asm.org/.
Present address: School of Veterinary Science, 250 Princes Highway, Werribee, Victoria 3030, Australia.
Present address: Bio21 Institute, Melbourne Dental School, 30 Flemington Rd., Parkville 3010, Australia.
Journal of Bacteriology, July 2009, p. 4111-4121, Vol. 191, No. 13
0021-9193/09/$08.00+0 doi:10.1128/JB.00251-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
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