title: The peritrophic matrix mediates differential infection outcomes in the tsetse fly gut following challenge with commensal, pathogenic, and parasitic microbes.
abstract: The insect gut is lined by a protective, chitinous peritrophic matrix (PM) that separates immunoreactive epithelial cells from microbes present within the luminal contents. Tsetse flies (Glossina spp.) imbibe vertebrate blood exclusively and can be exposed to foreign microorganisms during the feeding process. We used RNA interference-based reverse genetics to inhibit the production of a structurally robust PM and then observed how this procedure impacted infection outcomes after per os challenge with exogenous bacteria (Enterobacter sp. and Serratia marcescens strain Db11) and parasitic African trypanosomes. Enterobacter and Serratia proliferation was impeded in tsetse that lacked an intact PM because these flies expressed the antimicrobial peptide gene, attacin, earlier in the infection process than did their counterparts that housed a fully developed PM. After challenge with trypanosomes, attacin expression was latent in tsetse that lacked an intact PM, and these flies were thus highly susceptible to parasite infection. Our results suggest that immunodeficiency signaling pathway effectors, as opposed to reactive oxygen intermediates, serve as the first line of defense in tsetse's gut after the ingestion of exogenous microorganisms. Furthermore, tsetse's PM is not a physical impediment to infection establishment, but instead serves as a barrier that regulates the fly's ability to immunologically detect and respond to the presence of these microbes. Collectively, our findings indicate that effective insect antimicrobial responses depend largely upon the coordination of multiple host and microbe-specific developmental factors.
authors.affiliation: Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06520 brian.weiss@yale.edu.
authors.forename: Brian L
authors.initials: BL
authors.lastname: Weiss
authors.affiliation: Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06520.
authors.forename: Amy F
authors.initials: AF
authors.lastname: Savage
authors.affiliation: Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06520.
authors.forename: Bridget C
authors.initials: BC
authors.lastname: Griffith
authors.affiliation: Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06520.
authors.forename: Yineng
authors.initials: Y
authors.lastname: Wu
authors.affiliation: Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06520.
authors.forename: Serap
authors.initials: S
authors.lastname: Aksoy
mesh_terms: D000818:Animals; D002686:Chitin / Q000378:metabolism; D004754:Enterobacter / Q000276:immunology* / Q000502:physiology; D004847:Epithelial Cells / Q000276:immunology / Q000382:microbiology / Q000469:parasitology; D041981:Gastrointestinal Tract / Q000276:immunology* / Q000382:microbiology / Q000469:parasitology; D015870:Gene Expression / Q000276:immunology; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D054884:Host-Pathogen Interactions / Q000276:immunology; D019476:Insect Proteins / Q000235:genetics / Q000276:immunology / Q000378:metabolism; D008856:Microscopy, Fluorescence; D034622:RNA Interference; D051381:Rats; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012706:Serratia marcescens / Q000276:immunology* / Q000502:physiology; D015398:Signal Transduction / Q000235:genetics / Q000276:immunology; D014346:Trypanosoma brucei brucei / Q000276:immunology* / Q000502:physiology; D014370:Tsetse Flies / Q000235:genetics / Q000276:immunology* / Q000378:metabolism
chemical_list: D019476:Insect Proteins; C039711:attacin antibacterial protein, insect; D002686:Chitin; D049452:Green Fluorescent Proteins