The Impact of Environmental Habitats and Diets on the Gut Microbiota Diversity of True Bugs (Hemiptera: Heteroptera)

Abstract

Insects are generally associated with gut bacterial communities that benefit the hosts with respect to diet digestion, limiting resource supplementation, pathogen defense, and ecological niche expansion. Heteroptera (true bugs) represent one of the largest and most diverse insect lineages and comprise species consuming different diets and inhabiting various ecological niches, even including underwater. However, the bacterial symbiotic associations have been characterized for those basically restricted to herbivorous stink bugs of the infraorder Pentatomomorpha. The gut microbiota associated with the megadiverse heteropteran lineages and the implications of ecological and diet variance remain largely unknown. Here, we conducted a bacterial 16S rRNA amplicon sequencing of the gut microbiota across 30 species of true bugs representative of different ecological niches and diets. It was revealed that Proteobacteria and Firmicute were the predominant bacterial phyla. Environmental habitats and diets synergistically contributed to the diversity of the gut bacterial community of true bugs. True bugs living in aquatic environments harbored multiple bacterial taxa that were not present in their terrestrial counterparts. Carnivorous true bugs possessed distinct gut microbiota compared to phytophagous species. Particularly, assassin bugs of the family Reduviidae possessed a characterized gut microbiota predominantly composed of one Enterococcus with different Proteobacteria, implying a specific association between the gut bacteria and host. Overall, our findings highlight the importance of the comprehensive surveillance of gut microbiota association with true bugs for understanding the molecular mechanisms underpinning insect–bacteria symbiosis.

Diet and phylogeny shape the composition, diversity, and structure of the ant-gut bacterial community

“…Here, our results of CCA and RDA emphasized the importance of phylogeny through the level of in uence of both. It was also demonstrated that a recent study con rmed that at the species level, the differences in gut bacterial diversity were mainly determined by diet and environmental habitats [53]. Therefore, we speculate that ecological factors may be the main determinants of intestinal bacterial diversity in the lower taxonomic levels, while species phylogeny may play a greater role in the higher taxonomic levels.…”

“…A recent study has illustrated that the gut microbes of domesticated animals are more diverse than those of wild animals [13]. Secondly, the gut bacteria of some herbivorous true bugs are more diverse than those of carnivorous true bugs [53]. Thirdly, the gut bacteria of herbivorous insects that feed on plant juices and wood are more diverse than those of natural herbivores [15,54].…”

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

“…Based on the data from six Harpactorini species, Li and colleagues suggested Enterococcus bacteria to be a conserved microbiome component to most assassin bugs (50). In our data, Enterococcus is however only found in some individuals of Reduvius sp.…”

“…Similarly to Triatoma, host species was a significant predictor of assassin bug microbiome alpha (Supplementary Table S1-DATASHEET S12) and beta diversity (Figure 2, Supplementary Table S1 2A). Species specificity and a single taxon dominance resemble the microbiome characteristics of related hematophagous kissing bugs (11) but pose a sharp contrast to the recently published microbiome patterns in Old World assassins (50).…”

“…, Candidatus Midichloria in Stenolemoides arizonensis , and Zymobacter in Zelus longipes (Figure 2A). Species specificity and a single taxon dominance resemble the microbiome characteristics of related hematophagous kissing bugs (11) but pose a sharp contrast to the recently published microbiome patterns in Old World assassins (50). Based on the data from six Harpactorini species, Li and colleagues suggested Enterococcus bacteria to be a conserved microbiome component to most assassin bugs (50).…”