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Tokuda, G.

Publications and source records attributed to Tokuda, G..

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High-fidelity long-read metagenomics reveals the metabolic functions of dominant termite gut bacteria

Many termites digest lignocellulosic wood using diverse gut microbiota, yet functions are rarely linked to specific symbionts because complete genomes are scarce. We used PacBio HiFi long reads to reconstruct circular single-contig bacterial metagenome-assembled genomes (MAGs) from the gut microbiota of the wood-feeding termite Nasutitermes takasagoensis. From 13.9 Gb of HiFi data, we obtained highly contiguous assemblies, including 11 Breznakiellaceae (Spirochaetota), two Candidatus Fibrimonas (Fibrobacterota), and one Chitinispirillaceae genome, three dominant lineages in this gut ecosystem. The reconstructed genomes encoded extensive carbohydrate-active enzyme repertoires and anaerobic fermentation pathways consistent with lignocellulose degradation. They also carried genes for essential amino acid biosynthesis, while nitrogen-fixation capacity was present in representatives of all three lineages but varied among closely related strains. One Breznakiellaceae genome possessed a complete Wood-Ljungdahl pathway potentially supporting reductive acetogenesis in the presence of external formate, whereas related strains carried incomplete variants likely involved in anabolic C1 metabolism. Differences in CAZymes, C1 metabolism, and nitrogen fixation among closely related strains reveal functional diversification that fragmented MAGs would not resolve. The mapping of metatranscriptomic reads from three biological replicates of the fiber-associated community to the reconstructed genomes provided independent evidence that key predicted metabolic functions are transcriptionally active. Our results demonstrate the power of HiFi metagenomics to recover highly contiguous genomes from complex insect microbiomes and uncover lineage-specific metabolic roles of dominant termite gut symbionts.

microbiology↗

Convergent genetic rewiring of the brain underlies termite sociality

How genomes encode major transitions in social evolution is unclear. We use 29 near-chromosome-quality genomes across a spectrum of social complexity to explore the genomic basis of termite sociality. We show that shifts in selection and gene family evolution preceded the emergence of sociality, pointing to subtler genetic causes of this major evolutionary transition (MET). In comparisons of convergent societal forms, we find that a subset of Odorant Receptors (ORs) underwent parallel expansions in independent advanced termite societies displaying true worker phenotypes. The identified OR genes play caste-differentiated roles in termite but not nearest roach brains and are especially elaborated in true workers. Together with evidence of co-opted nutritional signaling and behavioral genes at different levels of social complexity, our study illuminates the rewiring of the molecular machinery underlying this MET.

genomics↗

Unravelling termite evolution with 47 high-resolution genome assemblies

Termites are a lineage of social cockroaches abundant in tropical ecosystems where they are key decomposers of organic matter from wood to soil. Despite their ecological significance, only a handful of reference-quality termite genomes have been sequenced, which is insufficient to unravel the genetic mechanisms that have contributed to their ecological success. Here, we performed sequencing and hybrid assembly of 45 taxonomically and ecologically diverse termites and two cockroaches, resulting in haplotype-merged genome assemblies of 47 species, 22 of which were near-chromosome level. Next, we examined the link between termite dietary evolution and major genomic events. We found that Termitidae, which include [~]80% of described termite species, have larger genomes with more genes and a higher proportion of transposons than other termites. Our analyses identified a gene number expansion early in the evolution of Termitidae, including an expansion of the repertoire of CAZymes, the genes involved in lignocellulose degradation. Notably, this expansion of genomes and gene repertoires coincided with the origin of soil-feeding in Termitidae and remained unchanged in lineages that secondarily reverted to a wood-based diet. Overall, our sequencing effort multiplied the number of available termite genomes by six and provided unprecedented insights into the genome evolution of the most ancient lineage of social insects.

genomics↗

The functional evolution of termite gut microbiota

Termites primarily feed on lignocellulose or soil in association with specific gut microbes. The functioning of the termite gut microbiota is partly understood in a handful of wood-feeding pest species, but remains largely unknown in other taxa. We intend to feel this gap and provide a global understanding of the functional evolution of termite gut microbiota. We sequenced the gut metagenomes of 145 samples representative of the termite diversity. We show that the prokaryotic fraction of the gut microbiota of all termites possesses similar genes for carbohydrate and nitrogen metabolisms, in proportions varying with termite phylogenetic position and diet. The presence of a conserved set of gut prokaryotic genes implies that key nutritional functions were present in the ancestor of modern termites. Furthermore, the abundance of these genes largely correlated with the host phylogeny. Finally, we found that the adaptation to a diet of soil by some termite lineages was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes and pathways. Our results reveal that the composition and function of termite gut prokaryotic communities have been remarkably conserved since termites first appeared [~]150 million years ago. Therefore, the "world smallest bioreactor" has been operating as a multipartite symbiosis composed of termites, archaea, bacteria, and cellulolytic flagellates since its inception.

evolutionary biology↗

Genomic and transcriptomic analyses of the subterranean termite Reticulitermes speratus: gene duplication facilitates social evolution

Termites are model social organisms characterized by a polyphenic caste system. Subterranean termites (Rhinotermitidae) are ecologically and economically important species, including acting as destructive pests. Rhinotermitidae occupies an important evolutionary position within the clade representing an intermediate taxon between the higher (Termitidae) and lower (other families) termites. Here, we report the genome, transcriptome and methylome of the Japanese subterranean termite Reticulitermes speratus. The analyses highlight the significance of gene duplication in social evolution in this termite. Gene duplication associated with caste-biased gene expression is prevalent in the R. speratus genome. Such duplicated genes encompass diverse categories related to social functions, including lipocalins (chemical communication), cellulases (wood digestion and social interaction), lysozymes (social immunity), geranylgeranyl diphosphate synthase (social defense) and a novel class of termite lineage-specific genes with unknown functions. Paralogous genes were often observed in tandem in the genome, but the expression patterns were highly variable, exhibiting caste biases. Some duplicated genes assayed were expressed in caste-specific organs, such as the accessory glands of the queen ovary and frontal glands in soldier heads. We propose that gene duplication facilitates social evolution through regulatory diversification leading to caste-biased expression and subfunctionalization and/or neofunctionalization that confers caste-specialized functions. Significance StatementTermites are model social organisms characterized by a sophisticated caste system, where distinct castes arise from the same genome. Our genomics data of Japanese subterranean termite provides insights into the evolution of the social system, highlighting the significance of gene duplication. Gene duplication associated with caste-biased gene expression is prevalent in the termite genome. Many of the duplicated genes were related to social functions, such as chemical communication, social immunity and defense, and they often expressed in caste-specific organs. We propose that gene duplication facilitates social evolution through regulatory diversification leading to caste-biased expression and functional specialization. In addition, since subterranean termites are ecologically and economically important species including destructive pests in the world, our genomics data serves as a foundation for these studies.

genomics↗