Tripartite interactions among kissing bugs, their gut-dwelling microorganisms, and the parasite Trypanosoma cruzi

The single-celled parasite Trypanosoma cruzi alternates between mammalian and insect hosts to complete its lifecycle. Humans infected with T. cruzi develop Chagas disease, a debilitating infection potentially resulting in severe cardiomyopathy estimated to affect 7 million people in Latin America. While promiscuous in its ability to infect a variety of mammalian hosts, T. cruzi exclusively is acquired and transmitted by blood-feeding insects of the subfamily Triatominae, the kissing bugs. Extracellular life stages of T. cruzi colonize the kissing bug gastrointestinal tract from which they are fecally transmitted back to vertebrate hosts. Because T. cruzi infection of insects is chronic, the parasite is forced to contend with the gut-dwelling microorganisms - the gut microbiota - of its kissing bug host long-term.

We hypothesize that T. cruzi and the microbiota compete for resources and space within the bug gut. To test this hypothesis, we firstly tracked bacteria and parasite populations in in vivo and in vitro settings. We determined that T. cruzi Y strain suppresses gut microbial proliferation in the kissing bug Rhodnius prolixus following blood ingestion. We further found that T. cruzi inhibits growth of the major kissing bug symbiont R. rhodnii when co-cultured in vitro. We next examined whether T. cruzi is in turn negatively affected by the gut microbiota by infecting microbe-free insects alongside conventionally reared controls, and found that parasitemia is significantly higher when insect gut microbes are absent. Taken together, our results provide strong evidence that T. cruzi and the kissing bug microbiota are mutually antagonistic.