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Applied and Environmental Microbiology, August 2009, p. 5250-5260, Vol. 75, No. 16
0099-2240/09/$08.00+0     doi:10.1128/AEM.00877-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Genetic Diversity and Multihost Pathogenicity of Clinical and Environmental Strains of Burkholderia cenocepacia {triangledown} ,{dagger}

A. Cody Springman,1,2,{ddagger} Janette L. Jacobs,1,3,{ddagger} Vishal S. Somvanshi,1,4,{ddagger} George W. Sundin,1,3 Martha H. Mulks,1,4 Thomas S. Whittam,1,2,§ Poorna Viswanathan,4 R. Lucas Gray,4 John J. LiPuma,5 and Todd A. Ciche1,4*

Center for Microbial Pathogenesis,1 National Food Safety and Toxicology Center,2 Department of Plant Pathology,3 Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48824,4 Department of Pediatrics and Communicable Diseases, University of Michigan, Ann Arbor, Michigan5

Received 17 April 2009/ Accepted 16 June 2009

A collection of 54 clinical and agricultural isolates of Burkholderia cenocepacia was analyzed for genetic relatedness by using multilocus sequence typing (MLST), pathogenicity by using onion and nematode infection models, antifungal activity, and the distribution of three marker genes associated with virulence. The majority of clinical isolates were obtained from cystic fibrosis (CF) patients in Michigan, and the agricultural isolates were predominantly from Michigan onion fields. MLST analysis resolved 23 distinct sequence types (STs), 11 of which were novel. Twenty-six of 27 clinical isolates from Michigan were genotyped as ST-40, previously identified as the Midwest B. cenocepacia lineage. In contrast, the 12 agricultural isolates represented eight STs, including ST-122, that were identical to clinical isolates of the PHDC lineage. In general, pathogenicity to onions and the presence of the pehA endopolygalacturonase gene were detected only in one cluster of related strains consisting of agricultural isolates and the PHDC lineage. Surprisingly, these strains were highly pathogenic in the nematode Caenorhabditis elegans infection model, killing nematodes faster than the CF pathogen Pseudomonas aeruginosa PA14 on slow-kill medium. The other strains displayed a wide range of pathogenicity to C. elegans, notably the Midwest clonal lineage which displayed high, moderate, and low virulence. Most strains displayed moderate antifungal activity, although strains with high and low activities were also detected. We conclude that pathogenicity to multiple hosts may be a key factor contributing to the potential of B. cenocepacia to opportunistically infect humans both by increasing the prevalence of the organism in the environment, thereby increasing exposure to vulnerable hosts, and by the selection of virulence factors that function in multiple hosts.


* Corresponding author. Mailing address: Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824. Phone: (517) 884-5359. Fax: (517) 353-8957. E-mail: ciche{at}msu.edu

{triangledown} Published ahead of print on 19 June 2009.

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

{ddagger} These authors contributed equally to this work.

§ Deceased.


Applied and Environmental Microbiology, August 2009, p. 5250-5260, Vol. 75, No. 16
0099-2240/09/$08.00+0     doi:10.1128/AEM.00877-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.