Host-specific assemblages typify gut microbial communities of related insect species

Abstract

Mutualisms between microbes and insects are ubiquitous and facilitate exploitation of various trophic niches by host insects. Dictyopterans (mantids, cockroaches and termites) exhibit trophisms that range from omnivory to strict wood-feeding and maintain beneficial symbioses with the obligate endosymbiont, Blattabacterium, and/or diverse gut microbiomes that include cellulolytic and diazotrophic microbes. While Blattabacterium in omnivorous Periplaneta is fully capable of provisioning essential amino acids, in wood-feeding dictyopterans it has lost many genes for their biosynthesis (Mastotermes and Cryptocercus) or is completely absent (Heterotermes). The conspicuous functional degradation and absence of Blattabacterium in most strict wood-feeding dictyopteran insects suggest that alternative means of acquiring nutrients limited in their diet are being employed. A 16S rRNA gene amplicon resequencing approach was used to deeply sample the composition and diversity of gut communities in related dictyopteran insects to explore the possibility of shifts in symbiont allegiances during termite and cockroach evolution. The gut microbiome of Periplaneta, which has a fully functional Blattabacterium, exhibited the greatest within-sample operational taxonomic unit (OTU) diversity and abundance variability than those of Mastotermes and Cryptocercus, whose Blattabacterium have shrunken genomes and reduced nutrient provisioning capabilities. Heterotermes lacks Blattabacterium and a single OTU that was 95% identical to a Bacteroidia-assigned diazotrophic endosymbiont of an anaerobic cellulolytic protist termite gut inhabitant samples consistently dominates its gut microbiome. Many host-specific OTUs were identified in all host genera, some of which had not been previously detected, indicating that deep sampling by pyrotag sequencing has revealed new taxa that remain to be functionally characterized. Further analysis is required to uncover how consistently detected taxa in the cockroach and termite gut microbiomes, as well as the total community, contribute to host diet choice and impact the fate of Blattabacterium in dictyopterans.Electronic supplementary materialThe online version of this article (doi:10.1186/2193-1801-3-138) contains supplementary material, which is available to authorized users.

Insect Gut Bacterial Diversity Determined by Environmental Habitat, Diet, Developmental Stage, and Phylogeny of Host

“…When bacterial abundances in different developmental stages were compared, anaerobe abundances were significantly higher in the larval stages than in adults (P ϭ 0.0034). Additionally, anaerobes were more abundant in the guts of omnivorous and Blattaria insects, which is supported by a previous report showing that dictyopteran insects, such as cockroaches and termites, have larger proportions of anaerobic Bacteroidia and Clostridia species (39).…”

The holobiont concept: the case of xylophagous termites and cockroaches

“…The genome of Blattabacterium strains isolated from the termite Mastotermes or from the cockroach Cryptocercus lacks most of the genes encoding the enzymes of metabolic pathways required for the synthesis of essential amino acids; this is in contrast to the genomes of Blattabacterium harbored by other cockroaches (Sabree et al 2012;Sabree and Moran 2014). Thus, additional members of the complex gut microbiota of the insects must compensate for this deficit and provide their hosts with the missing essential amino acids (Sabree and Moran 2014).…”

Molecular investigation of Australian termites and their gut symbionts

“…A study by Sabree and Moran (Sabree and Moran, 2014) using similar DNA extraction method and primers to ours produced a similar gut community profile for Mastotermes (Appendix A: Figure S2.12).…”

“…Two other important OTUs that were abundant in all Mastotermes samples despite the compositional shifts observed in some phyla were OTU57 (~10%) and OTU97 (~4%) assigned to Blattabacterium and Fusobacterium respectively (Figure 3.6 and Appendix B: (Sabree and Moran, 2014). Another gut symbiont, Fusobacterium, has been reported in almost all investigated Mastotermes gut profiles (3-6%) (Sabree et al, 2012;Sabree and Moran, 2014) Since it is well established that there are associations between the protist-symbiont bacterial phyla to hindgut protists (i.e.…”

“…Another gut symbiont, Fusobacterium, has been reported in almost all investigated Mastotermes gut profiles (3-6%) (Sabree et al, 2012;Sabree and Moran, 2014) Since it is well established that there are associations between the protist-symbiont bacterial phyla to hindgut protists (i.e. decrease in Elusimicrobia and Euryarchaeota), protist-symbiont prokaryotes could provide a gauge for evaluating the presence and absence of protists in lower termites as observed in the community composition shifts from time zero to day seven (Ohkuma, 2008 are capable of adapting to dietary changes over a short period of seven days (Geib et al, 2008;Husseneder et al, 2009;Sethi et al, 2012;Raychoudhury et al, 2013), it is still unclear when the gut microbial community composition alters to accommodate a new diet.…”