Physicochemical conditions, metabolites and community structure of the bacterial microbiota in the gut of wood-feeding cockroaches (Blaberidae: Panesthiinae)

Abstract

While the gut microbiota of termites and its role in symbiotic digestion have been studied for decades, little is known about the bacteria colonizing the intestinal tract of the distantly related wood-feeding cockroaches (Blaberidae: Panesthiinae). Here, we show that physicochemical gut conditions and microbial fermentation products in the gut of Panesthia angustipennis resemble that of other cockroaches. Microsensor measurements confirmed that all gut compartments were anoxic at the center and had a slightly acidic to neutral pH and a negative redox potential. While acetate dominated in all compartments, lactate and hydrogen accumulated only in the crop. The high, hydrogen-limited rates of methane emission from living cockroaches were in agreement with the restriction of F420-fluorescent methanogens to the hindgut. The gut microbiota of both P. angustipennis and Salganea esakii differed strongly between compartments, with the highest density and diversity in the hindgut, but similarities between homologous compartments of both cockroaches indicated a specificity of the microbiota for their respective habitats. While some lineages were most closely related to the gut microbiota of omnivorous cockroaches and wood- or litter-feeding termites, others have been encountered also in vertebrates, reinforcing the hypothesis that strong environmental selection drives community structure in the cockroach gut.

Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach, Diploptera punctata

“…Previous studies have characterized microbial communities of cockroaches, primarily the gut microbiome. Consistent with our findings, Bacteroidetes, Firmicutes, Proteobacteria, and unclassified bacteria are repeatedly found to be prominent members of adult cockroach endosymbiont communities (Bauer et al, ; Bertino‐Grimaldi et al, ; Carrasco et al, ; Gontang et al, ; Kakumanu, Maritz, Carlton, & Schal, ; Pérez‐Cobas et al, ; Schauer, Thompson, & Brune, ; Tinker & Ottesen, ). Similar to our adult female samples, other studies have shown Porphyromonadaceae, Rikenellaceae, and Bacteroidaceae to be the most abundant families of Bacteroidetes; while Lachnospiraceae, Ruminococcaceae, Clostridiaceae, and Lactobacillaceae are commonly represented Firmicutes (Bauer et al, ; Bertino‐Grimaldi et al, ; Carrasco et al, ; Gontang et al, ; Kakumanu et al, ; Pérez‐Cobas et al, ; Sabree & Moran, ; Schauer et al, ; Tinker & Ottesen, ).…”

The Gut Microbiota of Termites: Digesting the Diversity in the Light of Ecology and Evolution

“…The guts of cockroaches are colonized by ingestion of bacteria acquired from the environment, either together with the food source or by coprophagy (53,69,70), which introduces a strong stochastic element into habitat selection and would explain the highly similar yet individually variable community structure of cockroaches (2,99,105). In termites, however, proctodeal trophallaxis adds another deterministic component that attenuates the stochastic element by ensuring a reliable transfer of symbionts across generations and allows reciprocal adaptations that create host specificity and may eventually lead to cospeciation.…”

Deterministic Assembly of Complex Bacterial Communities in Guts of Germ-Free Cockroaches

“…In comparison, their closest relatives, the noneusocial cockroaches, do not depend on colony members for nourishment and can be raised in isolation under axenic conditions (9). Moreover, the physicochemical conditions in cockroach guts (5,10) are similar to those of many termites (11,12), which would offer a surrogate environment at least for those core lineages of gut microbiota that are shared with termites (5,6,13). These characteristics make cockroaches excellent models to experimentally test theories on the selective role of the insect gut environment in the assembly of the intestinal microbial community.…”