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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.

SUBMITTER: Xu 徐焕 H

PROVIDER: S-EPMC8599053 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The eusocial termites are well accomplished in chemical communication, but how they achieve the communication using trace amount of no more than two pheromone components is mostly unknown. In this study, the foraging process and trail pheromones of the fungus-growing termite Odontotermes formosanus (Shiraki) were systematically studied and monitored in real-time using a combination of techniques, including video analysis, solid-phase microextraction, gas chromatography coupled with either mass spectrometry or an electroantennographic detector, and bioassays. The trail pheromone components in foraging workers were (3Z)-dodec-3-en-1-ol and (3Z,6Z)-dodeca-3,6-dien-1-ol secreted by their sternal glands. Interestingly, ratio of the two components changed according to the behaviors that the termites were displaying. This situation only occurs in termites whereas ratios of pheromone components are fixed and species-specific for other insect cuticular glands. Moreover, in bioassays, the active thresholds of the two components ranged from 1 fg/cm to 10 pg/cm according to the behavioral contexts or the pheromonal exposure of tested workers. The two components did not act in synergy. (3Z)-Dodec-3-en-1-ol induced orientation behavior of termites that explore their environment, whereas (3Z,6Z)-dodeca-3,6-dien-1-ol had both an orientation effect and a recruitment effect when food was discovered. The trail pheromone of O. formosanus was regulated both quantitatively by the increasing number of workers involved in the early phases of foraging process, and qualitatively by the change in ratio of the two pheromone components on sternal glandular cuticle in the food-collecting workers. In bioassays, the responses of workers to the pheromone were also affected by the variation in pheromone concentration and component ratio in the microenvironment. Thus, this termite could exchange more information with nestmates using the traces of the two trail pheromone components that can be easily regulated within a limited microenvironment formed by the tunnels or chambers.

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

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