OmpA-Mediated Biofilm Formation Is Essential for the Commensal Bacterium Sodalis glossinidius To Colonize the Tsetse Fly Gut

Abstract

Many bacteria successfully colonize animals by forming protective biofilms. Molecular processes that underlie the formation and function of biofilms in pathogenic bacteria are well characterized. In contrast, the relationship between biofilms and host colonization by symbiotic bacteria is less well understood. Tsetse flies (Glossina spp.) house 3 maternally transmitted symbionts, one of which is a commensal (Sodalis glossinidius) found in several host tissues, including the gut. We determined that Sodalis forms biofilms in the tsetse gut and that this process is influenced by the Sodalis outer membrane protein A (OmpA). Mutant Sodalis strains that do not produce OmpA (Sodalis ⌬OmpA mutants) fail to form biofilms in vitro and are unable to colonize the tsetse gut unless endogenous symbiotic bacteria are present. Our data indicate that in the absence of biofilms, Sodalis ⌬OmpA mutant cells are exposed to and eliminated by tsetse's innate immune system, suggesting that biofilms help Sodalis evade the host immune system. Tsetse is the sole vector of pathogenic African trypanosomes, which also reside in the fly gut. Acquiring a better understanding of the dynamics that promote Sodalis colonization of the tsetse gut may enhance the development of novel disease control strategies.

Pathogen-mediated manipulation of arthropod microbiota to promote infection

“…Because A. phagocytophilum colonization reduced the abundance of Gram-positive biofilm-forming species like the Enterococci, we hypothesized that IAFGP alters the tick microbiota by inhibiting bacterial biofilms in the gut. Biofilms have been demonstrated to serve important roles in facilitating pathogen colonization in arthropod intestines (12)(13)(14). To elucidate the importance of IAFGP in shaping the tick gut microbiota, we injected the antibiofilm peptide, P1, derived from IAFGP (25), and showed that this improved A. phagocytophilum infection, in ticks.…”

“…The microbiota of arthropods and mammals has long been associated with robust biofilms (12,28). To further explore whether altering the biofilm has an effect on the whole tick gut microbial community, we compared the microbiota profiles of P1-injected and sP1-injected ticks.…”

“…In arthropods, the microbiota is associated with a biofilm, generated from diverse bacterial species. These microbial biofilms are necessary for establishing successful symbiotic relationships with their arthropod hosts (12)(13)(14).…”

Interwoven Biology of the Tsetse Holobiont

“…Notably, Sodalis has modified its outer membrane protein A (OmpA), which represents a molecular adaptation that contributes to host immune tolerance (68). The OmpA protein is also utilized in biofilm production within the tsetse gut, further protecting Sodalis from host immune responses (69).…”

Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug

“…Second, the defect in biofilm formation was another in vitro phenotype exhibited by the purL mutant (Figure 2c). Bacterial biofilm formation is one of the adaptation mechanisms to various environments and has been reported to be required for chronic infections and symbioses (Costerton et al, 2003;Ramey et al, 2004;Visick, 2009;An and Grewal, 2010;Burmølle et al, 2010;Morris and Visick, 2010;Rinaudi and Giordano, 2010;Maltz et al, 2012). In squid-Vibrio symbiosis, Vibrio fischeri uses a transient biofilm to colonize its host, Euprymna scolope (Visick, 2009;Morris and Visick, 2010).…”