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Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites.

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PubMed ID: 30504145

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Tokuda G, Mikaelyan A, Fukui C, Matsuura Y, Watanabe H, Fujishima M, Brune A

Proc Natl Acad Sci U S A. 12 2018. doi: 10.1073/pnas.1810550115

COMMENT: This study investigates the role of the fiber-associated microbial populations in the hindgut of higher termites in wood decomposition and elucidates the principal participants involved in hemicellulose degradation.

OBJECTIVES:

To clarify the role of bacterial symbionts in lignocellulose degradation in higher termites.

To explore the origin and function of genes encoding the major hemicellulolytic enzymes in the hindgut. 

MAIN RESULTS:

Xylanase activity was essentially confined to the hindgut proper.

When we compared xylanase activities with cellulolytic activities in the hindgut, we found that xylanase activities were in the same range as cellulolytic activities against carboxymethylcellulose (CMC) and more than an order of magnitude higher than activities against microcrystalline cellulose.

To identify genes involved in hemicellulose degradation activity detected in the hindgut compartment, we carried out a metatranscriptomic analysis (...) The majority of glycoside hydrolase (GH) transcripts expressed by the fiber-associated bacterial community belong to family GH11, which consists exclusively of xylanases. 

Metagenomic sequencing of the bacterial community associated with the fiber fraction yielded 126,962 contigs from more than 40 million reads. (...) Two of the contigs contained a complete GH11 gene (83% and 88% nucleotide sequence identity to Transcript 30253), in each case surrounded by genes with highest sequence similarity to those in Spirochaetes. Most of them were from Treponema primitia and Treponema azotonutricium, which are the only members of the Treponema I clade that have sequenced genomes and inhabit the hindgut of lower termites.

A horizontal transfer of the xylanase genes from Firmicutes to Spirochaetes (Nasutitermes cluster I) is supported by the results of metagenomic binning, which assigned the xylan-binding CBM36 modules associated with the corresponding GH11 xylanase genes or transcripts exclusively to Spirochaetes (bin 2).

CONCLUSIONS: 

Based on the correlation between diet and bacterial community structure in the hindguts of higher termites, the present study strongly suggests that the horizontal acquisition of novel digestive capacities by resident gut bacteria provided the termite host with the flexibility to exploit additional feeding substrates and eventually resulted in compositional changes in the entire hindgut microbiota.

Contributor

Raquel Ruiz-Arroyo