IDH knockdown alters foraging behavior in the termite Odontotermes formosanus in different social contexts

Abstract

Foraging, as an energy-consuming behavior, is very important for colony survival in termites. How energy metabolism related to glucose decomposition and adenosine triphosphate (ATP) production influences foraging behavior in termites is still unclear. Here, we analyzed the change in energy metabolism in the whole organism and brain after silencing the key metabolic gene isocitrate dehydrogenase (IDH) and then investigated its impact on foraging behavior in the subterranean termite Odontotermes formosanus in different social contexts. The IDH gene exhibited higher expression in the abdomen and head of O. formosanus. The knockdown of IDH resulted in metabolic disorders in the whole organism. The dsIDH-injected workers showed significantly reduced walking activity but increased foraging success. Interestingly, IDH knockdown altered brain energy metabolism, resulting in a decline in ATP levels and an increase in IDH activity. Additionally, the social context affected brain energy metabolism and, thus, altered foraging behavior in O. formosanus. We found that the presence of predator ants increased the negative influence on the foraging behavior of dsIDH-injected workers, including a decrease in foraging success. However, an increase in the number of nestmate soldiers could provide social buffering to relieve the adverse effect of predator ants on worker foraging behavior. Our orthogonal experiments further verified that the role of the IDH gene as an inherent factor was dominant in manipulating termite foraging behavior compared with external social contexts, suggesting that energy metabolism, especially brain energy metabolism, plays a crucial role in regulating termite foraging behavior.

Evolution of the sex-determination geneDoublesexwithin the termite lineage

“…Gene expression levels of Dsx homologs were measured using the Thunderbird SYBR qPCR Mix (Toyobo) and the MiniOpticon Real-time PCR system (Bio-Rad, Hercules, CA, USA) ( G. satsumensis and O. formosanus ) or the QuantStudio 3 Real-Time PCR System (Thermo Fisher Scientific) ( Z. nevadensis and H. sjostedti ). To determine an internal control gene, according to previous studies (Gao et al, 2020; Masuoka et al, 2015; Oguchi et al, 2022; Terrapon et al, 2014; Xu et al, 2021), the suitability of reference genes was evaluated using GeNorm (Vandesompele et al, 2002) and NormFinder (Andersen et al, 2004) software (Table S3). Gene-specific primers were designed using Primer3Plus (Untergasser et al, 2007) (Table S2).…”

Involvement of a catalase gene in lignin catalysis and immune defense against pathogenic fungus in Coptotermes formosanus: a potential new target for termite control

“…37 The entomopathogenic fungus M. anisopliae, widely used agent for biological pest control, has the potential for termite biological control. 38,39 Therefore, we used injection-type RNA interference (RNAi) technology to determine the contribution of Cfcat to lignin digestion in termites in vivo, and to explore how Cfcat affects the intestinal and systemic immune defense of termites against M. anisopliae.…”