Submitted to: Proceedings of the National Academy of Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/16/2010
Publication Date: 6/10/2010
Publication URL: http://handle.nal.usda.gov/10113/57353
Citation: Hughes, D.T., Terekhova, D.A., Liou, L., Hovde, C.J., Sahl, J.W., Patankar, A.V., Gonzalez, J.E., Edrington, T.S., Rasko, D.A., Sperandio, V. 2010. Chemical sensing in mammalian host-bacterial commensal associations. Proceedings of the National Academy of Sciences. 107:9831-9836. Interpretive Summary: A wide variety of bacteria live within the gastrointestinal system of cattle. These bacteria use a complex chemical sensing system to communicate with one another and possibly with the host animal. Bacteria, like E. coli O157:H7, respond to specific chemical signals produced by other bacteria within the animal. This research demonstrated that E. coli O157:H7 requires a specific chemical sensing compound, Sdi-A, to colonize within cattle. Interfering with this system of communication may be a means to prevent or reduce colonization of cattle by E. coli O157:H7.
Technical Abstract: The mammalian gastrointestinal (GI) tract is colonized by a complex consortium of bacterial species. Bacteria engage in chemical signaling to coordinate population-wide behavior. However, it is unclear if chemical sensing plays a role in establishing mammalian host–bacterial commensal relationships. Enterohemorrhagic Escherichia coli (EHEC) is a deadly human pathogen but is a member of the GI flora in cattle, its main reservoir. EHEC harbors SdiA, a regulator that senses acyl-homoserine lactones (AHLs) produced by other bacteria. Here, we show that SdiA is necessary for EHEC colonization of cattle and that AHLs are prominent within the bovine rumen but absent in other areas of the GI tract. We also assessed the rumen metagenome of heifers, and we show that it is dominated by Clostridia and/or Bacilli but also harbors Bacteroidetes. Of note, some members of the Bacteroidetes phyla have been previously reported to produce AHLs. SdiA-AHL chemical signaling aids EHEC in gauging these GI environments and promotes adaptation to a commensal lifestyle. We show that chemical sensing in the mammalian GI tract determines the niche specificity for colonization by a commensal bacterium of its natural animal reservoir. Chemical sensing may be a general mechanism used by commensal bacteria to sense and adapt to their mammalian hosts. Additionally, because EHEC is largely prevalent in cattle herds, interference with SdiA-mediated cattle colonization is an exciting alternative to diminish contamination of meat products and cross-contamination of produce crops because of cattle shedding of this human pathogen.