Comparison Between Worker and Soldier Transcriptomes of Termite Neotermes binovatus Reveals Caste Specialization of Host–Flagellate Symbiotic System

Termites are eusocial insects with functionally specialized workers and soldiers, both sharing the same genotype. Additionally, lower termites host flagellates in their hindguts that assist in wood digestion. However, worker-biased and soldier-biased gene expression patterns of the host-flagellate symbiotic system remain underexplored in most taxonomic groups. In this study, we sequenced high-depth transcriptomes from the workers and soldiers of a lower termite, <i>Neotermes binovatus</i> (Kalotermitidae), to investigate the differentially expressed termite transcripts, flagellate transcript abundance, and co-expression patterns of the host-flagellate transcript pairs in both castes. The worker-biased transcripts were enriched in functions related to cuticle development, nervous system regulation, pheromone biosynthesis, and metabolism, whereas the soldier-biased transcripts were predominantly involved in muscle development and kinesis, body morphogenesis, protein modification, and aggression. Flagellate transcripts from the orders Cristamonadida, Trichomonadida, Tritrichomonadida, and Oxymonadida were identified in both workers and soldiers, with the abundance of most flagellate transcripts tending to be higher in workers than in soldiers. Furthermore, we observed a much larger number of strong co-expression correlations between the termite and flagellate transcripts in workers than in soldiers, suggesting the possibility that soldiers depend more on food processed by worker holobionts than on their own symbiotic system. This research provides insights into the functional specialization of the host-flagellate symbiotic system in the worker and soldier castes of termites, supporting the workers' roles in nest maintenance, preliminary food processing, and communication, while emphasizing the defensive role of soldiers. Additionally, it offers new perspectives on the potential termite-flagellate interactions and underscores the need for whole-genome data of termite flagellates in further studies.