Biofilm Formation and Phenotypic Variation Enhance Predation-Driven Persistence of Vibrio cholerae

Persistence of the opportunistic bacterial pathogen Vibrio cholerae in aquatic environments is the principal cause for seasonal occurrence of cholera epidemics. This causality has been explained by postulating that V. cholerae forms biofilms in association with animate and inanimate surfaces. Altern...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2005-11, Vol.102 (46), p.16819-16824
Main Authors: Carsten Matz, Diane Mc Dougald, Ana Maria Moreno, Pui Yi Yung, Yildiz, Fitnat H., Kjelleberg, Staffan
Format: Article
Language:English
Subjects:
Bacteria
Biofilms
Biological Sciences
Cholera
Epidemics
Genotype & phenotype
Grazing
Mortality
Pathogens
Phenotype
Phenotypes
Physical Sciences
Plankton
Predation
Protozoan enzymes
Quorum sensing
Vibrio cholerae
Vibrio cholerae - pathogenicity
Vibrio cholerae - physiology
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Summary:Persistence of the opportunistic bacterial pathogen Vibrio cholerae in aquatic environments is the principal cause for seasonal occurrence of cholera epidemics. This causality has been explained by postulating that V. cholerae forms biofilms in association with animate and inanimate surfaces. Alternatively, it has been proposed that bacterial pathogens are an integral part of the natural microbial food web and thus their survival is constrained by protozoan predation. Here, we report that both explanations are interrelated. Our data show that biofilms are the protective agent enabling V. cholerae to survive protozoan grazing while their planktonic counterparts are eliminated. Grazing on planktonic V. cholerae was found to select for the biofilm-enhancing rugose phase variant, which is adapted to the surface-associated niche by the production of exopolymers. Interestingly, grazing resistance in V. cholerae biofilms was not attained by exopolymer production alone but was accomplished by the secretion of an antiprotozoal factor that inhibits protozoan feeding activity. We identified that the cell density-dependent regulator hapR controls the production of this factor in biofilms. The inhibitory effect of V. cholerae biofilms was found to be widespread among toxigenic and non-toxigenic isolates. Our results provide a mechanistic explanation for the adaptive advantage of surface-associated growth in the environmental persistence of V. cholerae and suggest an important contribution of protozoan predation in the selective enrichment of biofilm-forming strains in the out-of-host environment.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0505350102