The Role of Bacterial Symbionts in Triatomines: An Evolutionary Perspective

Abstract

Insects have established mutualistic symbiotic interactions with microorganisms that are beneficial to both host and symbiont. Many insects have exploited these symbioses to diversify and expand their ecological ranges. In the Hemiptera (i.e., aphids, cicadas, and true bugs), symbioses have established and evolved with obligatory essential microorganisms (primary symbionts) and with facultative beneficial symbionts (secondary symbionts). Primary symbionts are usually intracellular microorganisms found in insects with specialized diets such as obligate hematophagy or phytophagy. Most Heteroptera (true bugs), however, have gastrointestinal (GI) tract extracellular symbionts with functions analogous to primary endosymbionts. The triatomines, are vectors of the human parasite, Trypanosoma cruzi. A description of their small GI tract microbiota richness was based on a few culturable microorganisms first described almost a century ago. A growing literature describes more complex interactions between triatomines and bacteria with properties characteristic of both primary and secondary symbionts. In this review, we provide an evolutionary perspective of beneficial symbioses in the Hemiptera, illustrating the context that may drive the evolution of symbioses in triatomines. We highlight the diversity of the triatomine microbiota, bacterial taxa with potential to be beneficial symbionts, the unique characteristics of triatomine-bacteria symbioses, and the interactions among trypanosomes, microbiota, and triatomines.

Keywords: Chagas disease; Hemiptera; Trypanosoma; microbiome; microbiota; symbiosis; triatomines.

Figure 1

Evolutionary relationships among the four Hemiptera suborders and some selected Heteroptera. Hemipterans are divided taxonomically into four monophyletic suborders: Sternorrhyncha (i.e., aphids, psyllids, and whiteflies), Auchenorrhyncha (i.e., cicadas, spittlebugs, and planthoppers), Coleorrhyncha (i.e., moss bugs), and Heteroptera, (i.e., true tugs). Among the Heteroptera, the infraorders Pentatomomorpha (i.e., stinkbugs and firebugs) and Cimicomorpha (i.e., bed bugs, and triatomines) present symbioses with extracellular GI tract bacteria. Phylogenetic relationships were drawn based on [81,82].

Figure 2

The predominant bacteria from the GI tract of triatomines. Bacteria that represent over 1% of microbiomes from triatomine GI tracts belong to the phylum Bacteroidetes (5 genera in the clade in grey), Actinobacteria (14 genera in the clade in purple), Firmicutes (12 genera in the clade in red), and Proteobacteria (33 genera in the clade in green). Bacteria classes with only 1 representative genus are colored in black. The presence of these bacteria in different triatomines is shown as circles on the right side. Dominant bacteria (1%–3% of a microbiome) are represented with small circles and highly dominant bacteria (>3% of a microbiome) are represented with larger circles. The family Nocardiaceae and the order Enterobacteriales have many highly abundant bacteria. Intracellular bacteria are marked with a *. Data to build this figure were taken from [9,74,233,234,235,236,237,238,239,240,241,242,243]. The phylogenetic tree depicting the evolutionary relationships among bacteria was modified after retrieval from the NCBI taxonomy tool.