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Journal of Bacteriology, September 2004, p. 6015-6024, Vol. 186, No. 18
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.18.6015-6024.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Involvement of a Plasmid-Encoded Type IV Secretion System in the Plant Tissue Watersoaking Phenotype of Burkholderia cenocepacia

Amanda S. Engledow,1 Enrique G. Medrano,1,{dagger} Eshwar Mahenthiralingam,2 John J. LiPuma,3 and Carlos F. Gonzalez1*

Department of Plant Pathology & Microbiology, Texas A&M University, College Station, Texas,1 Cardiff School of Biosciences, Cardiff University, Cardiff, Wales, United Kingdom,2 Department of Pediatrics and Communicable Diseases, University of Michigan Medical School, Ann Arbor, Michigan3

Received 23 April 2004/ Accepted 16 June 2004

Burkholderia cenocepacia strain K56-2, a representative of the Burkholderia cepacia complex, is part of the epidemic and clinically problematic ET12 lineage. The strain produced plant tissue watersoaking (ptw) on onion tissue, which is a plant disease-associated trait. Using plasposon mutagenesis, mutants in the ptw phenotype were generated. The translated sequence of a disrupted gene (ptwD4) from a ptw-negative mutant showed homology to VirD4-like proteins. Analysis of the region proximal to the transfer gene homolog identified a gene cluster located on the 92-kb resident plasmid that showed homology to type IV secretion systems. The role of ptwD4, ptwC, ptwB4, and ptwB10 in the expression of ptw activity was determined by conducting site-directed mutagenesis. The ptw phenotype was not expressed by K56-2 derivatives with a disruption in ptwD4, ptwB4, or ptwB10 but was observed in a derivative with a disruption in ptwC. Complementation of ptw-negative K56-2 derivatives in trans resulted in complete restoration of the ptw phenotype. In addition, analysis of culture supernatants revealed that the putative ptw effector(s) was a secreted, heat-stable protein(s) that caused plasmolysis of plant protoplasts. A second chromosomally encoded type IV secretion system with complete homology to the VirB-VirD system was identified in K56-2. Site-directed mutagenesis of key secretory genes in the VirB-VirD system did not affect expression of the ptw phenotype. Our findings indicate that in strain K56-2, the plasmid-encoded Ptw type IV secretion system is responsible for the secretion of a plant cytotoxic protein(s).

* Corresponding author. Mailing address: Department of Plant Pathology & Microbiology, Texas A&M University, 2132 TAMU, College Station, TX 77843. Phone: (979) 845-7610. Fax: (979) 845-6483. E-mail: cf-gonzalez{at}tamu.edu.

{dagger} Present address: Cotton Pathology Research Laboratory, USDA, ARS, SPARC, College Station, TX 77845.

Journal of Bacteriology, September 2004, p. 6015-6024, Vol. 186, No. 18
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.18.6015-6024.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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