Campylobacter jejuni bile exposure influences outer membrane vesicles protein content and bacterial interaction with epithelial cells

Abstract

Campylobacter jejuni is a prevalent human pathogen and a major cause of bacterial gastroenteritis in the world. In humans, C. jejuni colonizes the intestinal tract and its tolerance to bile is crucial for bacteria to survive and establish infection. C. jejuni produces outer membrane vesicles (OMVs) which have been suggested to be involved in virulence. In this study, the proteome composition of C. jejuni OMVs in response to low concentration of bile was investigated. We showed that exposure of C. jejuni to low concentrations of bile, similar to the concentration in cecum, induced significant changes in the protein profile of OMVs released during growth without affecting the protein profile of the bacteria. This suggests that bile influences a selective packing of the OMVs after bacterial exposure to low bile. A low concentration of bile was found to increase bacterial adhesion to intestinal epithelial cells, likely by an enhanced hydrophobicity of the cell membrane following exposure to bile. The increased bacterial adhesiveness was not associated with increased invasion, instead bile exposure decreased C. jejuni invasion. OMVs released from bacteria upon exposure to low bile showed to increase both adhesion and invasion of non-bile-exposed bacteria into intestinal epithelial cells. These findings suggest that C. jejuni in environments with low concentrations of bile produce OMVs that facilitates colonization of the bacteria, and this could potentially contribute to virulence of C. jejuni in the gut.

Sodium Taurocholate Stimulates Campylobacter jejuni Outer Membrane Vesicle Production via Down-Regulation of the Maintenance of Lipid Asymmetry Pathway

“…Both the mlaA mutant OMVs and wild-type ST-OMVs had comparable diameters. This is in contrast to data from a recent study (Taheri et al, 2018) which did not observe increased OMV production in response to ox bile. Ox bile was used to represent a mixture of bile salts, similar to what would be found in the gut, whereas ST alone was used in this study, a single component of human bile.…”

Biofilm formation and extracellular microvesicles—The way of foodborne pathogens toward resistance

“…[185] indirectly confirmed the abovementioned findings by Taheri et al. [184] using bile salt sodium taurocholate. After treatment with this bile salt, C. jejuni outer MV production increased, with increased MVs‐associated proteolytic activity as a consequence.…”

“…According to Taheri et al [176] composition of the C. jejuni MVs depends on growth temperature and it has implications for the outcome of colonization and pathogenicity of this bacterium in different hosts. Elmi et al [185] indirectly confirmed the abovementioned findings by Taheri et al [184] using bile salt sodium taurocholate. After treatment with this bile salt, C. jejuni outer MV production increased, with increased MVs-associated proteolytic activity as a consequence.…”

“…Proteomics analyses have demonstrated that C. jejuni MVs contain proteins from the periplasm, outer membrane-associated proteins, as well as cytoplasmic proteins that are essential for both survival and pathogenesis of this foodborne bacterium [176,177,183]. Cleavage of host cells' proteins E-cadherin and occludin enhance bacterial invasion into host epithelial cells [181,182], and MVs isolated from in vitro bile treated bacteria also enhance this process [184]. According to Taheri et al [176] composition of the C. jejuni MVs depends on growth temperature and it has implications for the outcome of colonization and pathogenicity of this bacterium in different hosts.…”

Cracking Open Bacterial Membrane Vesicles

“…In addition, a similar route of MV formation has been suggested in Stenotrophomonas maltophilia, as production of O-IMVs and phages was detected in response to ciprofloxacin stress (Devos et al, 2017). The involvement of cell lysis in MV formation would explain why inner membrane and cytoplasmic components are detected in many proteomic analyses of OMV fractions (Kulkami et al, 2014;Olaya-Abril et al, 2014;Oliver et al, 2017;Avila-Calderón et al, 2018;Taheri et al, 2018).…”