Spatially selective colonization of the arthropod intestine through activation of Vibrio cholerae biofilm formation

Abstract

Vibrio cholerae is an estuarine bacterium and the human pathogen responsible for the diarrheal disease cholera. In the environment, arthropods are proposed to be carriers and reservoirs of V. cholerae. However, the molecular basis of the association between V. cholerae and viable arthropods has not been elucidated previously. Here, we show that the V. cholerae Vibrio polysaccharide (VPS)-dependent biofilm is highly activated upon entry into the arthropod intestine and is specifically required for colonization of the arthropod rectum. Although the V. cholerae VPS-dependent biofilm has been studied in the laboratory for many years, the function of this biofilm in the natural habitats of V. cholerae has been elusive. Our results provide evidence that the VPS-dependent biofilm is required for intestinal colonization of an environmental host.ach year, thousands of people living without access to adequate sanitation facilities contract cholera by ingesting food or water that carries the pandemic Vibrio cholerae bacillus (1). After passing through the acidic barrier of the stomach, V. cholerae replicates rapidly in the human gastrointestinal tract and ultimately leaves the body at concentrations as high as 10 9 per mL in a fast-developing, voluminous diarrhea characteristic of the disease. Release of trillions of bacteria into the environment from a single host results in rapid epidemic spread. Once the disease reaches a particular locale, it can become endemic to the region for years, reflecting the ability of V. cholerae to persist in the environment.Both pathogenic and nonpathogenic members of the diverse species of V. cholerae, which comprises more than 200 serogroups, are part of the normal aquatic microbial assemblage in the temperate coastal marine and estuarine waters of the world (2). In these environments, culture-dependent and culture-independent analyses have found V. cholerae in association with marine organisms such as fish (3) and copepods (4, 5). That V. cholerae can also be carried by insects such as chironomids (6) hints that V. cholerae interactions with arthropods are extensive. Indeed, V. cholerae has been isolated from houseflies in areas where cholera is endemic (7-12), signifying that both terrestrial and aquatic arthropods may act as disease reservoirs. Although the presence of arthropods has been correlated with cholera epidemics, a specific interaction between V. cholerae and arthropods has not been described.Bacterial biofilm formation mediates colonization of both biotic and abiotic surfaces. The V. cholerae multilayer biofilm, which is dependent on elaboration of a matrix comprised of the Vibrio polysaccharide (VPS) and several matrix-associated proteins (13, 14), has long been hypothesized to play a role in environmental survival. However, because this biofilm has been studied only in laboratory media, concrete evidence for such a role is lacking.Here, we demonstrate that formation of the V. cholerae VPSdependent biofilm is highly activated upon entry into the fly intestine and absolutely...

Pathogen-mediated manipulation of arthropod microbiota to promote infection

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