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Distinctive Repertoire of Contingency Genes Conferring Mutation- Based Phase Variation and Combinatorial Expression of Surface Lipoproteins in Mycoplasma capricolum subsp. capricolum of the Mycoplasma mycoides Phylogenetic Cluster

Kim S. Wise,^1* Mark F. Foecking,¹ Kerstin Röske,^1, Young Jin Lee,^3, Young Moo Lee,^3,¶ Anup Madan,^4,|| and Michael J. Calcutt²

Department of Molecular Microbiology and Immunology,¹ Department of Veterinary Pathobiology, University of Missouri-Columbia, Columbia, Missouri 65212,² Molecular Structure Facility, University of California Davis, Davis, California 95616,³ Institute for Systems Biology, Seattle, Washington 98103-8904⁴

Received 17 February 2006/ Accepted 21 April 2006

The generation of surface variation among many divergent species of Mollicutes (mycoplasmas) occurs through stochastic expression patterns of diverse lipoprotein genes. The size and wide distribution of such variable gene sets in minimal (0.6- to 1.4-Mb) mycoplasmal genomes suggest their key role in the adaptation and survival of these wall-less monoderms. Diversity through variable genes is less clearly established among phylogenetically similar mycoplasmas, such as the Mycoplasma mycoides cluster of ruminant pathogens, which vary widely in host range and pathobiology. Using (i) genome sequences from two members of this clade, Mycoplasma capricolum subsp. capricolum and M. mycoides subsp. mycoides small colony biotype (SC), (ii) antibodies to specific peptide determinants of predicted M. capricolum subsp. capricolum gene products, and (iii) analysis of the membrane-associated proteome of M. capricolum subsp. capricolum, a novel set of six genes (vmcA to vmcF) expressing distinct Vmc (variable M. capricolum subsp. capricolum) lipoproteins is demonstrated. These occur at two separate loci in the M. capricolum subsp. capricolum genome, which shares striking overall similarity and gene synteny with the M. mycoides subsp. mycoides SC genome. Collectively, Vmc expression is noncoordinate and combinatorial, subject to a single-unit insertion/deletion in a 5' flanking dinucleotide repeat that governs expression of each vmc gene. All vmc genes share modular regions affecting expression and membrane translocation. In contrast, vmcA to vmcD genes at one locus express surface proteins with highly structured size-variable repeating domains, whereas vmcE to vmcF genes express products with short repeats devoid of predicted structure. These genes confer a distinctive, dynamic surface architecture that may represent adaptive differences within this important group of pathogens as well as exploitable diagnostic targets.

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

Present address: Institute for Medical Microbiology and Hygiene, University of Dresden, D-01307 Dresden, Germany.

Present address: Genome Center Proteomics Core, University of California, Davis, CA 95616.

^¶ Present address: 4937 Marlborough Way, Carmichael, CA 95608.

^|| Present address: 200-B Neurogenomics Research Lab, University of Iowa, Iowa City, IA 52246.

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