Ciliate-Vibrio cholerae interactions within a microbial loop: an experimental study

Macek, Miroslav; Carlos, Genevieve Cherube R.; Memije, P; Ramírez, Patricia

doi:10.3354/ame013257

Cited by 14 publications

(19 citation statements)

References 20 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The present study elucidates the role of a major mortality factor in natural microbial communities, predation by protozoans. The high elimination rates found for V. cholerae in planktonic ecosystems (29)(30)(31)(32) suggest a tight control of V. cholerae growth and survival by protozoan predation. These observations raise the question how long-term persistence and seasonal accumulation of V. cholerae are possible in aquatic environments despite the predatory control by protozoans.…”

Section: Discussionmentioning

confidence: 99%

Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae

Matz

McDougald

Moreno

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

300

282

View full text Add to dashboard Cite

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 nontoxigenic 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.grazing ͉ resistance ͉ protozoa ͉ quorum sensing E pidemics of cholera, an acute intestinal infection caused by toxigenic strains of the facultative pathogen Vibrio cholerae, are a major public health problem in developing countries around the globe. Both toxigenic and nontoxigenic strains of V. cholerae are natural inhabitants of a wide range of aquatic ecosystems, including estuarine and coastal waters, that provide the environmental reservoir of virulent V. cholerae strains (1). The fact that many environmental nontoxigenic strains carry virulence genes (2, 3) and that the occurrence of epidemics coincides with the increased prevalence of the causative V. cholerae strain in the aquatic environment (4, 5) supports the notion of an environmental origin of toxigenic V. cholerae clones. This view has led to the hypothesis that cholera epidemics are triggered by environmental factors and selective forces governing aquatic microbial communities. In recent years, studies on the ecology of V. cholerae have considerably increased our understanding of physical and biological parameters that influence the persistence of V. cholerae in the environment and hold the potential to predict the outbreak of cholera epidemics (6).As a member of the natural bacterioplankton community, V. cholerae is an integral part of the pelagic microbial food web and is thus constrained in its growth and survival by the predatory action of bacterivorous protists, so...

show abstract

Section: Discussionmentioning

confidence: 99%

Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae

Matz

McDougald

Moreno

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

300

282

View full text Add to dashboard Cite

show abstract

“…Due to the long history of coexistence of bacteria and bacterivorous predatory protists, bacteria have evolved a number of grazing resistance strategies [1]. Vibrio ( V. ) cholerae , the causative agent of cholera is a natural inhabitant of aquatic ecosystems, and its long-term persistence in the environment is dependent on resistance to predation [2]–[4]. Biofilm formation and aggregation has been suggested to be important for survival of most microorganisms [5]–[7] and to contribute to the environmental persistence of V. cholerae [8]–[10].…”

Section: Introductionmentioning

confidence: 99%

Relative Contributions of Vibrio Polysaccharide and Quorum Sensing to the Resistance of Vibrio cholerae to Predation by Heterotrophic Protists

2013

View full text Add to dashboard Cite

Protozoan grazing is a major mortality factor faced by bacteria in the environment. Vibrio cholerae, the causative agent of the disease cholera, is a natural inhabitant of aquatic ecosystems, and its survival depends on its ability to respond to stresses, such as predation by heterotrophic protists. Previous results show that grazing pressure induces biofilm formation and enhances a smooth to rugose morphotypic shift, due to increased expression of Vibrio polysaccharide (VPS). In addition to negatively controlling vps genes, the global quorum sensing (QS) regulator, HapR, plays a role in grazing resistance as the ΔhapR strain is efficiently consumed while the wild type (WT) is not. Here, the relative and combined contributions of VPS and QS to grazing resistance were investigated by exposing VPS and HapR mutants and double mutants in VPS and HapR encoding genes at different phases of biofilm development to amoeboid and flagellate grazers. Data show that the WT biofilms were grazing resistant, the VPS mutants were less resistant than the WT strain, but more resistant than the QS mutant strain, and that QS contributes to grazing resistance mainly in mature biofilms. In addition, grazing effects on biofilms of mixed WT and QS mutant strains were investigated. The competitive fitness of each strain in mixed biofilms was determined by CFU and microscopy. Data show that protozoa selectively grazed the QS mutant in mixed biofilms, resulting in changes in the composition of the mixed community. A small proportion of QS mutant cells which comprised 4% of the mixed biofilm biovolume were embedded in grazing resistant WT microcolonies and shielded from predation, indicating the existence of associational protection in mixed biofilms.

show abstract

“…For example, in the pathogens Pseudomonas aeruginosa and V. cholerae , QS regulates the production of toxins that have been shown to kill predators, resulting in grazing resistance (Matz et al , 2004, 2008). While several studies have assessed the interactions of protozoa and V. cholerae in the suspended state and planktonically in mesocosms (Macek et al , 1997; Worden, 2006), surprisingly little is known about the impact of protozoa on the occurrence of attached V. cholerae .…”

Section: Introductionmentioning

confidence: 99%

In situ grazing resistance of Vibrio cholerae in the marine environment

Erken

Weitere

Kjelleberg

et al. 2011

FEMS Microbiology Ecology

View full text Add to dashboard Cite

Previous laboratory experiments revealed that Vibrio cholerae A1552 biofilms secrete an antiprotozoal factor that prevents Rhynchomonas nasuta from growing and thus prevents grazing losses. The antiprotozoal factor is regulated by the quorum-sensing response regulator, HapR. Here, we investigate whether the antiprotozoal activity is ecologically relevant. Experiments were conducted in the field as well as under field-like conditions in the laboratory to assess the grazing resistance of V. cholerae A1552 and N16961 (natural frameshift mutation in hapR) biofilms to R. nasuta and Cafeteria roenbergensis. In laboratory experiments exposing the predators to V. cholerae grown in seawater containing high and low glucose concentrations, we determined that V. cholerae biofilms showed increased resistance towards grazing by both predators as glucose levels decreased. The relative resistance of the V. cholerae strains to the grazers under semi-field conditions was similar to that observed in situ. Therefore, the antipredator defense is environmentally relevant and not lost when biofilms are grown in an open system in the marine environment. The hapR mutant still exhibited some resistance to both predators and this suggests that V. cholerae may coordinate antipredator defenses by a combination of density-dependent regulation and environmental sensing to protect itself from predators in its natural habitat.

show abstract

Ciliate-Vibrio cholerae interactions within a microbial loop: an experimental study

Cited by 14 publications

References 20 publications

Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae

Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae

Relative Contributions of Vibrio Polysaccharide and Quorum Sensing to the Resistance of Vibrio cholerae to Predation by Heterotrophic Protists

In situ grazing resistance of Vibrio cholerae in the marine environment

Contact Info

Product

Resources

About