Identifying the core microbial community in the gut of fungus‐growing termites

Abstract

Gut microbes play a crucial role in decomposing lignocellulose to fuel termite societies, with protists in the lower termites and prokaryotes in the higher termites providing these services. However, a single basal subfamily of the higher termites, the Macrotermitinae, also domesticated a plant biomass-degrading fungus (Termitomyces), and how this symbiont acquisition has affected the fungus-growing termite gut microbiota has remained unclear. The objective of our study was to compare the intestinal bacterial communities of five genera (nine species) of fungus-growing termites to establish whether or not an ancestral core microbiota has been maintained and characterizes extant lineages. Using 454-pyrosequencing of the 16S rRNA gene, we show that gut communities have representatives of 26 bacterial phyla and are dominated by Firmicutes, Bacteroidetes, Spirochaetes, Proteobacteria and Synergistetes. A set of 42 genus-level taxa was present in all termite species and accounted for 56-68% of the species-specific reads. Gut communities of termites from the same genus were more similar than distantly related species, suggesting that phylogenetic ancestry matters, possibly in connection with specific termite genus-level ecological niches. Finally, we show that gut communities of fungus-growing termites are similar to cockroaches, both at the bacterial phylum level and in a comparison of the core Macrotermitinae taxa abundances with representative cockroach, lower termite and higher nonfungus-growing termites. These results suggest that the obligate association with Termitomyces has forced the bacterial gut communities of the fungus-growing termites towards a relatively uniform composition with higher similarity to their omnivorous relatives than to more closely related termites.

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

“…For the analysis of taxonomic composition, a representative phylotype from each of the OTUs in a sample was classified with the RDP classifier (19) implemented in the mothur software suite (20) at a confidence cutoff of 80%, using DictDb v. 3.0 as reference database (13). Genus level lineages were ranked by determining their cumulative contribution to the principal component analysis of the gut communities as previously described (6,21). Additionally, MorisitaHorn distances were calculated for the communities at the genus level and visualized using nonmetric multidimensional scaling (NMDS) with the vegan package (22) in the R statistical software suite (23).…”

Erratum: Divergent functional isoforms drive niche specialisation for nutrient acquisition and use in rumen microbiome

“…In contrast, microbial community profiling using 16S ribosomal RNA has revealed core communities can be defined for many environments (Turnbaugh et al, 2009;Lundberg et al, 2012;Creevey et al, 2014;Otani et al, 2014), indicating that niche specialisation of specific groups of organisms is somehow maintained even under the continued influence of horizontal gene transfer. One explanation may be that the horizontal acquisition of a single isoform of a novel gene is not enough to maintain a competitive advantage in fluctuating environmental conditions where a range of isoforms may be required to, for instance, maintain enzymatic activity (Stewart, 1976;Nevo, 2001).…”

Transitional Complexity of Social Insect Immunity

“…Indeed, recent studies have provided insights into the complimentary roles of innate immunity and gut microbiota. For example, bacteria with antimicrobial and fungal cell wall degradation properties are found to be present in termite gut and nest microbiotas Poulsen et al, 2014;Rosengaus et al, 2014) with higher abundances compared to their ancestral solitary cockroaches (Dietrich et al, 2014;Otani et al, 2014). In bees, a number of antimicrobial peptide-producing bacteria have been sequenced to show that they are selectively higher in abundance in bees compared to Drosophila (Wong et al, 2011 and references therein).…”

“…Due to the recent proliferation of insect microbiota studies, social insect gut microbial communities are evident to be more specialized and structured when compared to solitary insects (Sabree et al, 2012;Engel and Moran, 2013;Otani et al, 2014). Given these seemingly more specialized gut microbes, an appreciable number of defensive genes/peptides observed in the social insect genetic biome are of microbial origins (e.g., Koch and Schmid-Hempel, 2011;Engel and Moran, 2013).…”

“…If secretions or bacteria in these insect-associated communities are able to be shared among nestmates, for example through allogrooming or trophallaxis (Hamilton et al, 2011;Konrad et al, 2012), it is plausible that they would qualify as part of social immunity (see definition above), and hence the complex and intricate interactions between bacterial communities and their host immunity would change through the evolutionary transition from solitary to eusocial insects. To date, limited comparisons between solitary and social insect gut microbiotas have been conducted (Martinson et al, 2011;Dietrich et al, 2014;Otani et al, 2014), but none has investigated the differences in microbe-derived immunity between social and solitary insect microbiotas.…”