Different roles of host and habitat in determining the microbial communities of plant-feeding true bugs

Abstract

Background The true bugs (Heteroptera) occupy nearly all of the known ecological niches of insects. Among them, as a group containing more than 30,000 species, the phytophagous true bugs are making increasing impacts on agricultural and forestry ecosystems. Previous studies proved that symbiotic bacteria play important roles in these insects in fitting various habitats. However, it is still obscure about the evolutionary and ecological patterns of the microorganisms of phytophagous true bugs as a whole with comprehensive taxon sampling. Results Here, in order to explore the symbiotic patterns between plant-feeding true bugs and their symbiotic microorganisms, 209 species belonging to 32 families of 9 superfamilies had been sampled, which covered all the major phytophagous families of true bugs. The symbiotic microbial communities were surveyed by full-length 16S rRNA gene and ITS amplicons respectively for bacteria and fungi using the PacBio platform. We revealed that hosts mainly affect the dominant bacteria of symbiotic microbial communities, while habitats generally influence the subordinate ones. Thereafter, we carried out the ancestral state reconstruction of the dominant bacteria and found that dramatic replacements of dominant bacteria occurred in the early Cretaceous and formed newly stable symbiotic relationships accompanying the radiation of insect families. In contrast, the symbiotic fungi were revealed to be horizontally transmitted, which makes fungal communities distinctive in different habitats but not significantly related to hosts. Conclusions Host and habitat determine microbial communities of plant-feeding true bugs in different roles. The symbiotic bacterial communities are both shaped by host and habitat but in different ways. Nevertheless, the symbiotic fungal communities are mainly influenced by habitat but not host. These findings shed light on a general framework for future microbiome research of phytophagous insects.

Cladosporium—Insect Relationships

“…However, the taxonomic remarks are reported as collective data considering the occurrence of fungi in soil and in association with insect pests, which does not allow us to infer specific associations with the latter [180]. Likewise, in an investigation concerning plant-feeding true bugs (Heteroptera: Cimicomorpha and Pentatomomorpha) carried out in China, data were summarized with reference to the family, not allowing us to infer the associations of Cladosporium with every single bug species [181].…”

Geographical, seasonal, and growth-related dynamics of gut microbiota in a grapevine pest, Apolygus spinolae (Heteroptera: Miridae) Running title: Gut microbiota of a grapevine pest bug

“…Based on their anatomical features, members of the Miridae, or plant bugs, are not thought to be associated with any speci c gut symbiont. Recent studies, however, revealed that plant bugs possess diverse microorganisms in their gut [11][12][13][14][15], some of which are commonly found in or even speci c to host plant bug species [14].…”

Geographical, seasonal, and growth-related dynamics of gut microbiota in a grapevine pest, Apolygus spinolae (Heteroptera: Miridae)

“…Based on their anatomical features, members of the Miridae, or plant bugs, are not thought to be associated with any speci c gut symbionts. Recent studies, however, revealed that plant bugs possess diverse microorganisms in their gut [13][14][15][16][17], some of which are commonly found in or even speci c to host plant bug species [16].…”