Multi-omics of cockroaches infected with Salmonella Typhimurium identifies molecular signatures of vector colonization

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BACKGROUND: German cockroaches (Blattella germanica) are prevalent indoor pests that have long been associated with the spread of enteric human pathogens. Recent work investigating the relationship between these insects and Salmonella enterica serovar Typhimurium (S. Typhimurium), a model pathogen of global concern, demonstrated that S. Typhimurium colonizes the cockroach gut. S. Typhimurium has a broad host range, but mechanistic molecular insight into how ecologically relevant invertebrate hosts interact with this pathogen is lacking. Here, we applied a multi-omic (transcriptomic and proteomic) approach to infected cockroaches to examine the molecular variables that govern cockroach-borne S. Typhimurium transmission. RESULTS: Our results reveal enriched monocarboxylic acid transport and metabolism, increased long-chain fatty acid transport, increased triglyceride metabolism, and an increased response to reactive oxygen species and free radicals as host signatures of a metabolic shift in the cockroach gut during infection. Surprisingly, downregulation of the immune deficiency (IMD) pathway transcription factor relish, and upregulation of xenobiotic detoxification (glutathione-s-transferase) and known allergens (Blag5 & Blag8, myosin, tropomyosin) were also evident in infected guts. CONCLUSIONS: To our knowledge, this study is both the first omics study of enteric human pathogen infection in a cockroach vector and the first omics study of S. Typhimurium in an ecologically relevant insect host, representing a seminal contribution to the field of vector-borne infectious disease. This work provides novel fundamental knowledge regarding the response of insect hosts to S. Typhimurium infection and the evolution of vector-pathogen relationships with the potential to inform mitigation of the public health impacts of cockroaches.

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