Metabolomic profiling of ¹³ C-labelled cellulose digestion in a lower termite: insights into gut symbiont function

Abstract

Termites consume an estimated 3–7 billion tonnes of lignocellulose annually, a role in nature which is unique for a single order of invertebrates. Their food is digested with the help of microbial symbionts, a relationship that has been recognized for 200 years and actively researched for at least a century. Although DNA- and RNA-based approaches have greatly refined the details of the process and the identities of the participants, the allocation of roles in space and time remains unclear. To resolve this issue, a pioneer study is reported using metabolomics to chart the in situ catabolism of 13C-cellulose fed to the dampwood species Hodotermopsis sjostedti. The results confirm that the secretion of endogenous cellulases by the host may be significant to the digestive process and indicate that a major contribution by hindgut bacteria is phosphorolysis of cellodextrins or cellobiose. This study provides evidence that essential amino acid acquisition by termites occurs following the lysis of microbial tissue obtained via proctodaeal trophallaxis.

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

“…The gut can be described as an anaerobic gradient system which is constantly supplied with oxygen via the epithelium (Köhler et al 2012). The gut microbiota is commonly exchanged between colony members and transmitted to the next generation via trophallaxis (proctodeal feeding), which can promote coevolutional diversification of symbiotic microbes along with host phylogeny (Tokuda et al 2014). Termites comprise a complex assemblage of diverse species, roughly divided into lower and higher termites.…”

Molecular investigation of Australian termites and their gut symbionts

“…These genes encoding GHs from prokaryotic symbionts of two lower termite genera, Mastotermes and Porotermes, support potential involvement of prokaryotes in lignocellulose digestion, as recently reported in other lower termites (Mattéotti et al, 2012;Do et al, 2014;Tokuda et al, 2014;Peterson et al, 2015;Yuki et al, 2015). From the broad functional categories of GHs, all metagenomes had higher relative abundances of hemicellulases as compared to cellulases, one-fold higher in higher termites and four-fold higher in lower termites (Figure 4.4 and Appendix C: Table S4.2).…”

“…Recent work has shown possible cellulose digestion involvement of bacterial symbionts in lower termites via (1) genomic identification of genes related to lignocellulose degradation (Boucias et al, Do et al, 2014;Yuki et al, 2015), (2) antimicrobial treatments which suggest involvement of cellulolytic prokaryotes in metabolism of carbohydrate and phenolic components of lignocellulose (Peterson et al, 2015) and (3) metabolomic profiling of hindgut bacteria through phosphorolysis of cellobiose or cellodextrins (Tokuda et al, 2014). Though these studies have provided insights into the importance of gut prokaryotes in digestive processes, the involvement of these lignocellulose degrading genes in lower termites is still unclear.…”

[Dedicated to Prof. T. Okada and Prof. T. Nishioka: data science in chemistry]Visualizing Individual and Region-specific Microbial–metabolite Relations by Important Variable Selection Using Machine Learning Approaches

“…MNR also provides accurate quantification 10 with inter-institution convertibility 11 . In previous studies, NMR-based metabolic profiling has been applied to plants [12][13][14][15] , animals [16][17][18][19][20] , and microbial [21][22][23][24] systems.…”