Dominant ectosymbiotic bacteria of cellulolytic protists in the termite gut also have the potential to digest lignocellulose

Abstract

Wood-feeding lower termites harbour symbiotic gut protists that support the termite nutritionally by degrading recalcitrant lignocellulose. These protists themselves host specific endo- and ectosymbiotic bacteria, functions of which remain largely unknown. Here, we present draft genomes of a dominant, uncultured ectosymbiont belonging to the order Bacteroidales, 'Candidatus Symbiothrix dinenymphae', which colonizes the cell surface of the cellulolytic gut protists Dinenympha spp. We analysed four single-cell genomes of Ca. S. dinenymphae, the highest genome completeness was estimated to be 81.6-82.3% with a predicted genome size of 4.28-4.31 Mb. The genome retains genes encoding large parts of the amino acid, cofactor and nucleotide biosynthetic pathways. In addition, the genome contains genes encoding various glycoside hydrolases such as endoglucanases and hemicellulases. The genome indicates that Ca. S. dinenymphae ferments lignocellulose-derived monosaccharides to acetate, a major carbon and energy source of the host termite. We suggest that the ectosymbiont digests lignocellulose and provides nutrients to the host termites, and hypothesize that the hydrolytic activity might also function as a pretreatment for the host protist to effectively decompose the crystalline cellulose components.

Single-Cell Amplicon Sequencing Reveals Community Structures and Transmission Trends of Protist-Associated Bacteria in a Termite Host

“…It is generally accepted that at least some of the protist species are cellulolytic, which stems from the observations that some protists commonly contain wood particles in their cytoplasm (1) and some members, which were previously cultivated from another termite species, were shown to hydrolyze cellulose in vitro (49,50). There are recent reports that some ectosymbionts of Oxymonadida protists have the capacity to hydrolyze some of the polysaccharides found in wood (9,47). These include 'Ca.…”

“…Other known ectosymbionts include a Desulfovibrio species which embeds in the membrane of its host, Trichonympha (7). Functional and genomic data regarding the nature of these symbioses are limited but growing (8,9).…”

“…Other known ectosymbionts include a Desulfovibrio species which embeds in the membrane of its host, Trichonympha (7). Functional and genomic data regarding the nature of these symbioses are limited but growing (8,9).The endosymbionts which colonize the cytoplasm of hindgut protists of Reticulitermes termites are from several bacterial taxa and vary between protist and termite species. These include Endomicrobium (10), and 'Candidatus Ancillula' (11).…”

Metagenomic analyses highlight the symbiotic association between the glacier stonefly Andiperla willinki and its bacterial gut community

“…At least 67 susC-susD tandems were present in AwDysgo as seen in phylogenetically related 'Candidatus Symbiothrix dinenymphae' (Supporting Information Fig. S5A), an ectosymbiont of cellulolytic protists in the termite gut (Yuki et al, 2015). Several examples of the PULs in AwDysgo are shown in Supporting Information Fig.…”

Discovery and Complete Genome Sequence of a Bacteriophage from an Obligate Intracellular Symbiont of a Cellulolytic Protist in the Termite Gut

“…Termites feed exclusively on dead plant matter, and nutritionally depend on gut microbes, which play crucial roles in the digestion of lignocellulose and provision of nitrogenous compounds (7, 13, 19, 28, 45, 46). This symbiosis is multilayered, with cellulolytic gut protists harboring both endo- and ectosymbiotic bacteria (7, 13).…”