Transcriptional Response of the Termite Coptotermes formosanus to Infection by the Entomopathogenic Fungus Akanthomyces lecanii

Kai Feng; Qi Ye; Yiyang Zhao; Liang Liu; Yueqiu He; Wen Li; Feilong Yu; Zhilong Wang; Weigang Chai

doi:10.13102/sociobiology.v73i3.12316

Authors

Kai Feng College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Qi Ye College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Yiyang Zhao College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Liang Liu College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Yueqiu He College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Wen Li College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Feilong Yu College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Zhilong Wang College of Landscape and Ecology, NingBo City College of Vocational Technology, Ningbo 315000, China
Weigang Chai Ningbo Academy of Agricultural Sciences, Ningbo 315000, China

DOI:

https://doi.org/10.13102/sociobiology.v73i3.12316

Keywords:

termite, immune response, metabolism, fungal infection

Abstract

Coptotermes formosanus, a worldwide pest, inflicts large losses on agriculture, forestry, construction, and other industries. As efficient, environmentally friendly pest control methods, microbial biopesticides are widely used to manage major pests. We previously isolated an Akanthomyces lecanii strain with strong insecticidal activity against termites. However, the interaction between the biocontrol agent and termites is still unknown. In this study, PacBio single-molecule real-time (SMRT) sequencing technology and Illumina RNA-seq sequencing technology were used to explore the transcriptomic differences in C. formosanus before and after A. lecanii infection. A total of 7,882,407 full-length transcripts were obtained. Single genes were further annotated using the NR, GO, KEGG, COG/KOG, Swiss-Prot, and KEGG homology public databases. A total of 2,782 differentially expressed genes were identified, including 1,440 upregulated genes and 1,342 downregulated genes. The expression of the Toll signaling pathway, mitogen-activated protein kinase (MAPK) pathway, detoxification metabolism, and immune-related genes, including scavenger receptor, apolipophorin, Cdc42, Integrin, Toll, serine protease, and transferrin genes, may be related to A. lecanii infection. This work not only greatly enriches the gene annotation resources of C. formosanus but also provides a new perspective for understanding the fungal immune defense mechanisms of social insects at the molecular level. These findings provide a theoretical basis for the development of new immunosuppressive agents.

Downloads

Download data is not yet available.

References

Cassidy, S.T., Chapa, J., Tran, T.A., Dolezal, N., Gerena, C., Johnson, G., Leyva, A., Stein, S., Wright, C.M., & Keiser, C.N. (2021). Disease defences across levels of biological organization: individual and social immunity in acorn ants. Animal Behaviour, 179: 73-81.

Chen, W., & Li, Z. (2025). miR-571 manipulating termite immune response to fungus and showing potential for green management of Copotermes formosanus (Blattodea: Isoptera). Pesticide Biochemistry and Physiology, 208: 106274.

Chen, W.W., Zeng, W.H., Shen, D.N., Feng, S.Y., & Li, Z.Q. (2023). Genome-wide identification of Coptotermes formosanus immune genes and their potential roles in termite control. Gene, 877: 147569.

da Silva, L.H.B., Goes, A.C., Rodrigues, A., Fourcassié, V., McMahon, D., & Haifig, I. (2025). Social immune response reflects infection progression in a soldierless termite. Behavioral Ecology and Sociobiology, 79: 11.

de la Fuente, J., Blouin, E.F., Manzano-Roman, R., Naranjo, V., Almazan, C., Pérez de la Lastra, J.M., Zivkovic, Z., Jongejan, F., & Kocan, K.M. (2007). Functional genomic studies of tick cells in response to infection with the cattle pathogen, Anaplasma marginale. Genomics, 90: 712–22.

Eleftherianos, I., Heryanto, C., Bassal, T., Zhang, W., Tettamanti, G., & Mohamed, A. (2021). Haemocyte‐mediated immunity in insects: Cells, processes and associated components in the fight against pathogens and parasites. Immunology, 164: 401-432.

Feng, K., Jiang, D., Luo, J., & Tang, F. (2023). OfGNBP silencing enhances the toxicity of Serratia marcescens Bizio (SM1) to Odontotermes formosanus (Shiraki). Pesticide Biochemistry and Physiology, 189: 105306.

Feng, K., Lu, X., Luo, J., & Tang, F. (2020). SMRT sequencing of the full-length transcriptome of Odontotermes formosanus (Shiraki) under Serratia marcescens treatment. Scientific Reports, 10(1): 15909.

Gao, S., Ren, Y., Sun, Y., Wu, Z.F., Ruan, J.S., He, B.J., Zhang, T., Yu, X., Tian, X.X., & Bu, W.J. (2016). PacBio full-length transcriptome profiling of insect mitochondrial gene expression. RNA Biology, 13: 820-825.

Govind, S. (2008). Innate immunity in Drosophila: Pathogens and pathways. Insect Science, 15: 29-43.

Guo, Z., Kang, S., Wu, Q., Wang, S., Crickmore, N., Zhou, X., Bravo, A., Soberón, M., & Zhang, Y. (2021). The regulation landscape of MAPK signaling cascade for thwarting Bacillus thuringiensis infection in an insect host. PLoS Pathogens, 17: e1009917.

He, Y.J., Lu, G., Qi, Y.H., Zhang, Y., Zhang, X.D., Huang, H.J., Zhuo, J.C., Sun, Z.T., Yan, F., Chen, J.P., Zhang, C.X., & Li, J.M. (2021). Activation of Toll Immune Pathway in an Insect Vector Induced by a Plant Virus. Frontiers in Immunology, 11: 613957.

Hu, Y.X., Wang, Y., Deng, J.P., & Jiang, H.B. (2016). The structure of a prophenoloxidase (PPO) from Anopheles gambiae provides new insights into the mechanism of PPO activation. BMC Biology, 14: 2.

Ji, Y., Lu, T., Zou, Z., & Wang, Y. (2022). Aedes aegypti CLIPB9 activates prophenoloxidase-3 in the presence of CLIPA14 after fungal infection. Frontiers in Immunology, 13: 927322.

Jia, D., Wang, Y., Liu, Y., Hu, J., Guo, Y.Q., Gao, L.L., & Ma, R.Y. (2018). SMRT sequencing of full-length transcriptome of flea beetle Agasicles hygrophila (Selman and Vogt). Scientific Reports, 8: 2197.

Kalil, S.P., Rosa, R.D., Capelli-Peixoto, J., Pohl, P.C., Oliveira, P.L., Fogaça, A.C., & Daffre, S. (2017). Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale. Parasites & Vectors, 10: 613.

Kalleshwaraswamy, C.M., Shanbhag, R.R., & Sundararaj, R. (2022). Wood degradation by termites: Ecology, economics, and protection. Science of Wood Degradation and its Protection (pp.147-170). Singapore: Springer Singapore.

Kepler, R.M., Jennifer, L.A.J., Hywel-Jones, N.L., Quandt, C.A., Sung, G.H., Rehner, S.A., Aime, M.C., Henkel, T.W., Sanjuan, T., Zare, R., Chen, M.J., Li, Z.Z., Rossman, A.Y., Spatafora, J.W., & Shrestha, B. (2017). A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus, 8: 335-353.

Khan, S.A., & Han, Y.S. (2024). Current status of innate immune responses in Malpighian tubules of insects: A review focusing on the Toll signaling pathway. Entomological Research, 54: e12716.

Kojour, M.A.M., Han, Y.S., Hun, Y.J., & Jo, Y.H. (2020). An overview of insect innate immunity. Entomological Research, 50: 282–291.

Lee, S.B., Tong, R.L., Kim, S.H., Im, I.G., & Su, N.Y. (2021). Potential pest status of the Formosan subterranean termite, Coptotermes formosanus Shiraki (Blattodea: Isoptera: Rhinotermitidae), in response to climate change in the Korean Peninsula. Florida Entomologist, 103: 431-437.

Lemaitre, B., & Hoffmann, J. (2007). The host defense of Drosophila melanogaster. Annual Review of Immunology, 25: 697–743.

Liu, L., Yan, F.M., Zhao, C.C., Su, L.J., Huang, Q.Y., & Tang, Q.B. (2023). microRNAs shape social immunity: a potential target for biological control of the termite Reticulitermes chinensis. Journal of Pest Science, 96: 265-279.

Liu, Z.C., Zhou, L., Wang, J.L., & Liu, X.S. (2021). Expression of a phenoloxidase cascade inhibitor enhances the virulence of the fungus Beauveria bassiana against the insect Helicoverpa armigera. Developmental & Comparative Immunology, 117: 103986.

Mahanta, D.K., Bhoi, T.K., Komal, J., Samal, I., Nikhil, R.M., Paschapur, R.N., Singh, G., Kumar, P.V.D., Desai, D.R., Ahmad, M.A., Singh, P.P., Majhi, P.K., Mukherjee, U., Singh, P., Saini, V., Shahanaz, Srinivasa, N., & Yele, Y. (2023). Insect-pathogen crosstalk and the cellular-molecular mechanisms of insect immunity: uncovering the underlying signaling pathways and immune regulatory function of non-coding RNAs. Frontiers in Immunology, 14: 1169152.

Merkling, S.H., & van Rij, R.P. (2013). Beyond RNAi: antiviral defense strategies in Drosophila and mosquito. Journal of Insect Physiology, 59: 159–170.

Pili-Floury, S., Leulier, F., Takahashi, K., Saigo, K., Samain, E., Ueda, R., & Lemaitre, B. (2004). In Vivo RNA Interference Analysis Reveals an Unexpected Role for GNBP1 in the Defense against Gram-positive Bacterial Infection in Drosophila Adults. Journal of Biological Chemistry, 279: 12848–12853.

Sharma, A., Sharma, S., & Yadav, P.K. (2023). Entomopathogenic fungi and their relevance in sustainable agriculture: A review. Cogent Food & Agriculture, 9(1): 2180857.

Sharma, I., Sharma, A., & Sharma, S. (2025). Role of Termites in Waste Management: Current Progress and Future Potential. Waste Management: From Trash to Treasure, 125p.

Stanley, D., Haas, E., & Kim, Y. (2023). Beyond cellular immunity: on the biological significance of insect hemocytes. Cells, 12: 599.

Wang, J.H., Huang, J.S., & Fang, X.D. (2007). Identification and induction by Metarhizium anisopliae infection of family4 cytochrome P450in Brontispa longissimi. Acta Entomologica Sinica, 50: 14-19.

Wang, J.L., Yang, K.H., Wang, S.S., Li, X.L., Liu, J., Yu, Y.X., & Liu, X.S. (2022). Infection of the entomopathogenic fungus Metarhizium rileyi suppresses cellular immunity and activates humoral antibacterial immunity of the host Spodoptera frugiperda. Pest Management Science, 78: 2828-2837.

Xu, S., Duan, Y., Ma, L., Song, F., Tian, L., Cai, W.Z., & Li, H. (2023). Full-length transcriptome profiling of Coridius chinensis mitochondrial genome reveals the transcription of genes with ancestral arrangement in insects. Genes, 14: 225.

Xue, Y., Li, H., & Kang, X. (2024). Molecular unraveling of polysaccharide digestion in wood-feeding termites: A solid-state NMR perspective. Carbohydrate Polymers, 331: 121843.

Zeng, W., Shen, D., Wu, W., Zhang, S.J., Li, Z.Q., & Zhang, D.D. (2024). Involvement of a catalase gene in lignin catalysis and immune defense against pathogenic fungus in Coptotermes formosanus: a potential new target for termite control. Pest Management Science, 80: 3258-3268.