Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut

Abstract

Termites thrive on dead plant matters with the aid of microorganisms resident in their gut. The gut microbiota comprises protists (single-celled eukaryotes), bacteria, and archaea, most of which are unique to the termite gut ecosystem. Although this symbiosis has long been intriguing researchers of both basic and applied sciences, its detailed mechanism remains unclear due to the enormous complexity and the unculturability of the microbiota. In the effort to overcome the difficulty, recent advances in omics, such as metagenomics, metatranscriptomics, and metaproteomics have gradually unveiled the black box of this symbiotic system. Genomics targeting a single species of the unculturable microbial members has also provided a great progress in the understanding of the symbiotic interrelationships among the gut microorganisms. In this review, the symbiotic system organized by wood-feeding termites and their gut microorganisms is outlined, focusing on the recent achievement in omics studies of this multilayered symbiotic system.

Fig. 1

Termites and their intestinal tract. a The lower termites Coptotermes formosanus. b The interface (wood and humus)-feeding higher termites Termes comis. c The gut of C. formosanus. d The gut of T. comis. F foregut, M midgut. Bars = 1 mm

Fig. 2

Microbiota in the hindgut of termites. a Phase-contrast image of the microbiota in the gut of the lower termite Reticulitermes speratus. b Phase-contrast image of the microbiota in the gut of the lower termite Coptotermes formosanus. c Phase-contrast image of the microbiota in the wood-feeding higher termite Nasutitermes takasagoensis. d FISH (fluorescent in situ hybridization) image of c. Texas-red signals: treponemes; 6FAM (green) signals: a novel group (FibS2) of the phylum Fibrobacteres [72]. Amorphous yellow colors were autofluorescence emitted from wood particles. Bars = 100 μm in a and b and 10 μm in c and d

Fig. 3

Cellular symbiosis between gut protists and bacteria. a Phase-contrast image of the anterior region of the parabasalid protist Trichonympha agilis from the termite Reticulitermes speratus. b FISH (fluorescent in situ hybridization) image of a. Hair-like treponeme cells were specifically detected with 6FAM-labeled probes (green). c FISH image of a. Bristle-like Bacteroidales cells were specifically detected with a Texas red-labeled probe. d Phase-contrast image of T. agilis. e FISH image of d. Rs-D17 cells were specifically detected with a Texas red-labeled probe. Other bacterial cells were detected with a 6FAM-labeled probe (green). f Transmission electron micrograph of Rs-D17. g Phase-contrast image of the parabasalid protist Pseudotrichonympha grassii from the termite Coptotermes formosanus. h FISH image of a P. grassii cell. CfPt1-2 cells were specifically detected with a 6FAM-labeled probe (green). Bars = 20 μm in a–e; 0.5 μm in e; 50 μm in g; 10 μm in h. Panels a–c, d–f, and g–h were originally published in [107], [122], and [123], respectively, and slightly modified

Fig. 4

Schematic view of the multilayered symbiosis in the termite Coptotermes formosanus. The figure was originally published in [123] and modified here