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Genome of 'Ca. Desulfovibrio trichonymphae', an H2-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut.

ABSTRACT: The cellulolytic protist Trichonympha agilis in the termite gut permanently hosts two symbiotic bacteria, 'Candidatus Endomicrobium trichonymphae' and 'Candidatus Desulfovibrio trichonymphae'. The former is an intracellular symbiont, and the latter is almost intracellular but still connected to the outside via a small pore. The complete genome of 'Ca. Endomicrobium trichonymphae' has previously been reported, and we here present the complete genome of 'Ca. Desulfovibrio trichonymphae'. The genome is small (1?410?056?bp), has many pseudogenes, and retains biosynthetic pathways for various amino acids and cofactors, which are partially complementary to those of 'Ca. Endomicrobium trichonymphae'. An amino acid permease gene has apparently been transferred between the ancestors of these two symbionts; a lateral gene transfer has affected their metabolic capacity. Notably, 'Ca. Desulfovibrio trichonymphae' retains the complex system to oxidize hydrogen by sulfate and/or fumarate, while genes for utilizing other substrates common in desulfovibrios are pseudogenized or missing. Thus, 'Ca. Desulfovibrio trichonymphae' is specialized to consume hydrogen that may otherwise inhibit fermentation processes in both T. agilis and 'Ca. Endomicrobium trichonymphae'. The small pore may be necessary to take up sulfate. This study depicts a genome-based model of a multipartite symbiotic system within a cellulolytic protist cell in the termite gut.

SUBMITTER: Kuwahara H

PROVIDER: S-EPMC5322295 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Genome of 'Ca. Desulfovibrio trichonymphae', an H<sub>2</sub>-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut.

Kuwahara Hirokazu H Yuki Masahiro M Izawa Kazuki K Ohkuma Moriya M Hongoh Yuichi Y

The ISME journal 20161101 3

The cellulolytic protist Trichonympha agilis in the termite gut permanently hosts two symbiotic bacteria, 'Candidatus Endomicrobium trichonymphae' and 'Candidatus Desulfovibrio trichonymphae'. The former is an intracellular symbiont, and the latter is almost intracellular but still connected to the outside via a small pore. The complete genome of 'Ca. Endomicrobium trichonymphae' has previously been reported, and we here present the complete genome of 'Ca. Desulfovibrio trichonymphae'. The genom ...[more]

PMID: 27801909

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Project description:Fungus-growing termites are efficient in degrading and digesting plant substrates, achieved through the engagement of symbiotic gut microbiota and lignocellulolytic Termitomyces fungi cultivated for protein-rich food. Insights into where specific plant biomass components are targeted during the decomposition process are sparse. In this study, we performed several analytical approaches on the fate of plant biomass components and did amplicon sequencing of the 16S rRNA gene to investigate the lignocellulose digestion in the symbiotic system of the fungus-growing termite Odontotermes formosanus (Shiraki) and to compare bacterial communities across the different stages in the degradation process. We observed a gradual reduction of lignocellulose components throughout the process. Our findings support that the digestive tract of young workers initiates the degradation of lignocellulose but leaves most of the lignin, hemicellulose, and cellulose, which enters the fresh fungus comb, where decomposition primarily occurs. We found a high diversity and quantity of monomeric sugars in older parts of the fungus comb, indicating that the decomposition of lignocellulose enriches the old comb with sugars that can be utilized by Termitomyces and termite workers. Amplicon sequencing of the 16S rRNA gene showed clear differences in community composition associated with the different stages of plant biomass decomposition which could work synergistically with Termitomyces to shape the digestion process. IMPORTANCE Fungus-farming termites have a mutualist association with fungi of the genus Termitomyces and gut microbiota to support the nearly complete decomposition of lignocellulose to gain access to nutrients. This elaborate strategy of plant biomass digestion makes them ecologically successful dominant decomposers in (sub)tropical Old World ecosystems. We employed acid detergent fiber analysis, high-performance anion-exchange chromatography (HPAEC), high-performance liquid chromatography (HPLC), scanning electron microscopy (SEM), Fourier transform infrared spectroscopy (FTIR), X-ray diffraction (XRD), pyrolysis gas chromatography-mass spectrometry (Py-GC-MS), and amplicon sequencing of the 16S rRNA gene to examine which lignocellulose components were digested and which bacteria were abundant throughout the decomposition process. Our findings suggest that although the first gut passage initiates lignocellulose digestion, the most prominent decomposition occurs within the fungus comb. Moreover, distinct bacterial communities were associated with different stages of decomposition, potentially contributing to the breakdown of particular plant components.

Dataset Information

Genome of 'Ca. Desulfovibrio trichonymphae', an H2-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut.

Publications

Genome of 'Ca. Desulfovibrio trichonymphae', an H<sub>2</sub>-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut.

Similar Datasets

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