Fungiculture in Termites Is Associated with a Mycolytic Gut Bacterial Community

Abstract

Termites forage on a range of substrates, and it has been suggested that diet shapes the composition and function of termite gut bacterial communities. Through comparative analyses of gut metagenomes in nine termite species with distinct diets, we characterize bacterial community compositions and use peptide-based functional annotation method to determine biomass-degrading enzymes and the bacterial taxa that encode them. We find that fungus-growing termite guts have relatively more fungal cell wall-degrading enzyme genes, while wood-feeding termite gut communities have relatively more plant cell wall-degrading enzyme genes. Interestingly, wood-feeding termite gut bacterial genes code for abundant chitinolytic enzymes, suggesting that fungal biomass within the decaying wood likely contributes to gut bacterial or termite host nutrition. Across diets, the dominant biomass-degrading enzymes are predominantly coded for by the most abundant bacterial taxa, suggesting tight links between diet and gut community composition, with the most marked difference being the communities coding for the mycolytic capacity of the fungus-growing termite gut. IMPORTANCE Understanding functional capacities of gut microbiomes is important to improve our understanding of symbiotic associations. Here, we use peptide-based functional annotation to show that the gut microbiomes of fungus-farming termites code for a wealth of enzymes that likely target the fungal diet the termites eat. Comparisons to other termites showed that fungus-growing termite guts have relatively more fungal cell wall-degrading enzyme genes, whereas wood-feeding termite gut communities have relatively more plant cell wall-degrading enzyme genes. Across termites with different diets, the dominant biomass-degrading enzymes are predominantly coded for by the most abundant bacterial taxa, suggesting tight links between diet and gut community compositions.

A Study of the Gut Bacterial Community of Reticulitermes virginicus Exposed to Chitosan Treatment

“…Spirochaetes were also significantly lower in STV samples in comparison to all other samples. These results confirm the findings of Tokuda et al [ 54 ] that Spirochaetes have a very important role in the lignocellulose degradation of wood-feeding termites, while Bacteroidetes and Firmicutes bacteria appear to be very important in producing mycolytic enzymes in the hindgut of fungus-growing termites [ 55 ].…”

Symbiotic Plant Biomass Decomposition in Fungus-Growing Termites

“…The possible roles of gut bacteria in fungus-growing termites include decomposition of other parts of the ingested plant substrates [32,39,63,64], inhibition of pathogens [65], amino acid synthesis [66], and nitrogen fixation [64,67]. The guts of fungus-growing termites also have a greater abundance of enzymes targeting chitin [39,64,68] and other fungal cell wall components [39,63,68], possibly in part contributed by the bacteria dominating fungus-growing termite guts [39,63,67].…”

“…The breakdown of lignin may also be complemented by chemical reactions during the first gut passage [53]. Given that specific cleavage and removal of lignin has been documented in wood feeders [127,128], it may not be surprising that the fungus-growing termite symbiosis depolymerizes lignin structures, even though only a few lignin-targeting bacterial enzymes have been identified in the termite gut [39,68].…”

MCIC: Automated Identification of Cellulases From Metagenomic Data and Characterization Based on Temperature and pH Dependence

“…Firstly, raw data was prepared for samples in four different environments, including termite gut, soil, sheep rumen, and cattle rumen. Alongside a cattle rumen raw reads that was obtained from authors' another study (Gharechahi et al, 2020), three other samples were downloaded from NCBI's Short Read Archive (SRA) including termite sample (Whole genome shotgun sequencing of Macrotermes natalensis soldier gut metagenome) under accession number: SRR797686 (Hu et al, 2019), soil sample raw reads downloaded under accession number: ERR1939274 (Orellana et al, 2018), and sheep rumen with accession number SRR1222429 (Kamke et al, 2016). Reads quality was checked using FastQC tools, and reads with relatively poor quality (Phred score < 20)…”