The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its responses to dietary lignocellulose composition

Abstract

Reticulitermes flavipes (Isoptera: Rhinotermitidae) is a highly eusocial insect that thrives on recalcitrant lignocellulosic diets through nutritional symbioses with gut-dwelling prokaryotes and eukaryotes. In the R. flavipes hindgut, there are up to 12 eukaryotic protozoan symbionts; the number of prokaryotic symbionts has been estimated in the hundreds. Despite its biological relevance, this diverse community, to date, has been investigated only by culture- and cloning-dependent methods. Moreover, it is unclear how termite gut microbiomes respond to diet changes and what roles they play in lignocellulose digestion. This study utilized high-throughput 454 pyrosequencing of 16S V5-V6 amplicons to sample the hindgut lumen prokaryotic microbiota of R. flavipes and to examine compositional changes in response to lignin-rich and lignin-poor cellulose diets after a 7-day feeding period. Of the ~475,000 high-quality reads that were obtained, 99.9% were annotated as bacteria and 0.11% as archaea. Major bacterial phyla included Spirochaetes (24.9%), Elusimicrobia (19.8%), Firmicutes (17.8%), Bacteroidetes (14.1%), Proteobacteria (11.4%), Fibrobacteres (5.8%), Verrucomicrobia (2.0%), Actinobacteria (1.4%) and Tenericutes (1.3%). The R. flavipes hindgut lumen prokaryotic microbiota was found to contain over 4761 species-level phylotypes. However, diet-dependent shifts were not statistically significant or uniform across colonies, suggesting significant environmental and/or host genetic impacts on colony-level microbiome composition. These results provide insights into termite gut microbiome diversity and suggest that (i) the prokaryotic gut microbiota is much more complex than previously estimated, and (ii) environment, founding reproductive pair effects and/or host genetics influence microbiome composition.

The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae)

“…Bacteroidetes were found in low concentrations (1 %) in R. lucifugus, in contrast to the abundance found in Reticulitermes santonensis (Feytaud) (Yang et al 2005) and R. flavipes (Boucias et al 2013). Members of the phylum Bacteroidetes have been reported to reside in the gut as ecto-or endosymbionts of flagellated protozoa (Noda et al 2005;Nakajima et al 2006), and cellularlevel symbioses between Bacteroidales and gut protists are as common as those between spirochetes and gut protists.…”

Diversity and resilience of the wood‐feeding higher termite Mironasutitermes shangchengensis gut microbiota in response to temporal and diet variations

“…Much evidence suggests that the bacterial diversity of the gut microbiota is essential for maintaining gut homeostasis (Boucias et al., 2013; Hu, Lukasik, Moreau, & Russell, 2014). In the gut of Reticulitermes flavipes termites, a diet of corn stover reduced the bacterial richness and diversity, compared with sorghum and two other woody diets (Huang et al., 2013).…”

“…Firstly , the diet has significant effects on the gut microbiome of both lower and higher termites (Boucias et al., 2013; Huang, Bakker, Judd, Reardon, & Vivanco, 2013). For example, the gut bacterial community of the lower termite Reticulitermes flavipe can be differentiated on the basis of grassy and woody diets as well as among different grassy diets (Huang et al., 2013).…”

Linking lignocellulosic dietary patterns with gut microbial Enterotypes of Tsaitermes ampliceps and comparison with Mironasutitermes shangchengensis

“…Recent studies have indicated that different dietary habits shape the structure of microbiota in the termite gut (Boucias et al, 2013;Huang et al, 2013;Raychoudhury et al, 2013). Dietary manipulation induces measurable differences among gut bacterial communities, and the recalcitrance of plant substrates may be the major cause of this variation in the diversity and richness of gut bacterial communities (Boucias et al, 2013;Huang et al, 2013;Raychoudhury et al, 2013). However, influences on the abundance and diversity of the intestinal microbial of termite fed with different substrates containing various lignin and cellulose or hemicellulose remain unclear.…”

“…The diversity and complexity of the termite gut microbiota have been evaluated using molecular technology techniques based on 16S rRNA (Warnecke et al, 2007;Berlanga et al, 2011;Mathew et al, 2012). Recent studies have indicated that different dietary habits shape the structure of microbiota in the termite gut (Boucias et al, 2013;Huang et al, 2013;Raychoudhury et al, 2013). Dietary manipulation induces measurable differences among gut bacterial communities, and the recalcitrance of plant substrates may be the major cause of this variation in the diversity and richness of gut bacterial communities (Boucias et al, 2013;Huang et al, 2013;Raychoudhury et al, 2013).…”