Microbiomes of blood feeding triatomines in the context of their predatory relatives and the environment

Abstract

AbstractThe importance of gut microbiomes has become generally recognized in vector biology. This study addresses microbiome signatures in North AmericanTriatomaspecies of public health significance (vectors ofTrypanosoma cruzi) linked to their blood feeding strategy and the natural habitat. To place theTriatomaassociated microbiomes within a complex evolutionary and ecological context, we sampled sympatricTriatomapopulations, related predatory reduviids, unrelated ticks, and environmental material from vertebrate nests where these arthropods reside. Along with fiveTriatomaspecies, we have characterized microbiomes of five reduviids (Stenolemoides arizonensis,Ploiaria hirticornis,Zelus longipes, and twoReduviusspecies), a single soft tick species,Ornithodoros turicata,and environmental microbiomes from selected sites in Arizona, Texas, Florida and Georgia. The microbiomes of predatory reduviids lack a shared core microbiota. Like in triatomines, microbiome dissimilarities among species corelate with dominance of a single bacterial taxa. These includeRickettsia,Lactobacillus, CandidatusMidichloria, andZymobacter, which are often accompanied by known symbiotic genera, i.e.,Wolbachia,CandidatusLariskella,Asaia,Gilliamella, andBurkholderia.We have further identified compositional convergence of analyzed microbiomes in respect to the host phylogenetic distance in both blood feeding and predatory reduviids. While microbiomes of two reduviid species from Emesinae family reflect their close relationship, the microbiomes of allTriatomaspecies repeatedly form a distinct monophyletic cluster highlighting their phylosymbiosis. Furthermore, based on environmental microbiome profiles and blood meal analysis, we propose three epidemiologically relevant and mutually interrelated bacterial sources forTriatomamicrobiomes, i.e., host abiotic environment, host skin microbiome, and pathogens circulating in host blood.ImportanceThis study places microbiomes of blood feeding North AmericanTriatomavectors (Reduviidae) into a broader evolutionary and ecological context provided by related predatory assassin bugs (Reduviidae), another unrelated vector species (soft tickOrnithodor turicata), and the environment these arthropods cohabit. For both vectors, microbiome analyses suggest three interrelated sources of bacteria, i.e., microbiome of vertebrate nests as their natural habitat, vertebrate skin microbiome, and pathobiome circulating in vertebrate blood. Despite an apparent influx of environment-associated bacteria into the arthropod microbiomes,Triatomamicrobiomes retain their specificity, forming a distinct cluster that significantly differ from both predatory relatives and ecologically comparable ticks. Similarly, within the related predatory Reduviidae, we found the host phylogenetic distance to underlie microbiome similarities.