Metagenomic Insights into Metabolic Capacities of the Gut Microbiota in a Fungus-Cultivating Termite (Odontotermes yunnanensis)

Ning Liu,Zhihua Zhou,Qian Wang,Haokui Zhou,Lei Xie,Meiling Zhang,Lei Zhang,Shengyue Wang,Yongping Huang,Yanhua Long,Xing Yan,John Parkinson

doi:10.1371/journal.pone.0069184

Abstract

Macrotermitinae (fungus-cultivating termites) are major decomposers in tropical and subtropical areas of Asia and Africa. They have specifically evolved mutualistic associations with both a Termitomyces fungi on the nest and a gut microbiota, providing a model system for probing host-microbe interactions. Yet the symbiotic roles of gut microbes residing in its major feeding caste remain largely undefined. Here, by pyrosequencing the whole gut metagenome of adult workers of a fungus-cultivating termite (Odontotermes yunnanensis), we showed that it did harbor a broad set of genes or gene modules encoding carbohydrate-active enzymes (CAZymes) relevant to plant fiber degradation, particularly debranching enzymes and oligosaccharide-processing enzymes. Besides, it also contained a considerable number of genes encoding chitinases and glycoprotein oligosaccharide-processing enzymes for fungal cell wall degradation. To investigate the metabolic divergence of higher termites of different feeding guilds, a SEED subsystem-based gene-centric comparative analysis of the data with that of a previously sequenced wood-feeding Nasutitermes hindgut microbiome was also attempted, revealing that SEED classifications of nitrogen metabolism, and motility and chemotaxis were significantly overrepresented in the wood-feeder hindgut metagenome, while Bacteroidales conjugative transposons and subsystems related to central aromatic compounds metabolism were apparently overrepresented here. This work fills up our gaps in understanding the functional capacities of fungus-cultivating termite gut microbiota, especially their roles in the symbiotic digestion of lignocelluloses and utilization of fungal biomass, both of which greatly add to existing understandings of this peculiar symbiosis.

Highlights

Termites are notable for extensive plant biomass degradation capacity
Statistical Analysis To investigate the metabolic divergence of the gut microbiomes between fungus-grower and that of a previously sequenced woodfeeding Nasutitermes species [15], a gene-centric comparative analysis was conducted using abundance of environmental gene tags (EGTs) in each of the two dataset as a comparative metric, as described and applied in other cases [16,19,32]
Metagenomic reads annotated by SEED subsystems were defined as EGTs and approximately 30% of all obtained reads (Table 1) could be classified as EGTs which could be used for further gene-centric comparative analysis

Summary

Introduction

Termites are notable for extensive plant biomass degradation capacity. instead of providing all endogenous enzymes necessary for foodstuffs digestion, they have developed mutualistic symbiosis with versatile groups of microorganisms which are known to play essential roles for this process. Statistical Analysis To investigate the metabolic divergence of the gut microbiomes between fungus-grower and that of a previously sequenced woodfeeding Nasutitermes species [15], a gene-centric comparative analysis was conducted using abundance of EGTs in each of the two dataset as a comparative metric, as described and applied in other cases [16,19,32].

Results

Conclusion