Microbial Response to Fungal Infection in a Fungus-Growing Termite, Odontotermes formosanus (Shiraki)

The crosstalk between gut microbiota and host immunity has emerged as one of the research foci of microbiome studies in recent years. The purpose of this study was to determine how gut microbes respond to fungal infection in termites, given their reliance on gut symbionts for food intake as well as maintaining host health. Here, we used Metarhizium robertsii, an entomopathogenic fungus, to infect Odontotermes formosanus, a fungus-growing termite in the family Termitidae, and documented changes in host gut microbiota via a combination of bacterial 16S rDNA sequencing, metagenomic shotgun sequencing, and transmission electron microscopy. Our analyses found that when challenged with Metarhizium, the termite gut showed reduced microbial diversity within the first 12 h of fungal infection and then recovered and even surpassed pre-infection flora levels. These combined results shed light on the role of gut flora in maintaining homeostasis and immune homeostasis in the host, and the impact of gut flora dysbiosis on host susceptibility to infection.

In addition to cryptochrome 2, magnetic particles with olfactory co-receptor are important for magnetic orientation in termites

The volatile trail pheromone is an ephemeral chemical cue, whereas the geomagnetic field (GMF) provides a stable positional reference. However, it is unclear whether and how the cryptic termites perceive the GMF for orientation in light or darkness until now. Here, we found that the two termite species, Reticulitermes chinensis and Odontotermes formosanus, use the GMF for orientation. Our silencing cryptochrome 2 (Cry2) impaired magnetic orientation in white light but had no significant impact in complete darkness, suggesting that Cry2 can mediate magnetic orientation in termites only under light. Coincidentally, the presence of magnetic particles enabled the magnetic orientation of termites in darkness. When knock-downing the olfactory co-receptor (Orco) to exclude the effect of trail pheromone, unexpectedly, we found that the Orco participated in termite magnetic orientation under both light and darkness. Our findings revealed a novel magnetoreception model depending on the joint action of radical pair, magnetic particle, and olfactory co-receptor.

First Record of the Soil-feeding Higher Termites (Isoptera: Termitidae) from Okinawa Island, the Central Ryukyus, Japan

Some of termites have been introduced outside their native ranges, and it has been suggested that both wood-eating and wood-nesting lifestyles are critical for the transportation of propagules. Here, we present the first record of the soil-feeding and soil-nesting termite Pericapritermes nitobei (Isoptera: Termitidae) in the Motobu Peninsula on the northern part of Okinawa Island in the Central Ryukyus. The fact that the previous extensive surveys of termites in the Ryukyu Archipelago did not detect P. nitobei in the Central Ryukyus, including the Motobu Peninsula, and its discontinuous distribution, indicate that P. nitobei has been recently introduced into the Motobu Peninsula of Okinawa Island from the Yaeyama Islands, similar to the fungus-growing and soil-nesting termite Odontotermes formosanus (Isoptera: Termitidae). Together with O. formosanus in the southern part of Okinawa Island, our findings in this study raise the possibility that non-wood-feeding and non-wood-nesting termites can be introduced and established outside their native ranges by human activities.

Insecticidal Activities Against Odontotermes formosanus and Plutella xylostella and Corresponding Constituents of Tung Meal from Vernicia fordii

The environmental pollution, pesticide resistance, and other associated problems caused by traditional chemical pesticides with limited modes of action make it urgent to seek alternative environmentally-friendly pesticides from natural products. Tung meal, the byproduct of the detoxified Vernicia fordii (Hemsl.) seed, has been commonly used as an agricultural fertilizer and as a pesticide. However, its active insecticidal extracts and ingredients remain elusive. In the present study, the contact toxicities of tung meal extracts against the agricultural and forest pests like O. formosanus and P. xylostella were examined. Our results showed that ethyl acetate and petroleum ether extracts showed the strongest toxicity against O. formosanus and P. xylostella, respectively. In order to further explore the chemical profiles of the ethyl acetate and petroleum ether extracts, UPLC-Q/TOF-MS and GC-MS analyses have been performed, and 20 and 29 compounds were identified from EA and PE extracts, respectively. The present study, for the first time, verified the noteworthy insecticidal activities on the aforementioned agricultural and forest pesticides and revealed the potential active parts and chemical composition, which are conducive to further exploiting the potential of tung meal as a natural plant-derived insecticide for biological control of agricultural and forest pests.

Response of Three Kinds of Detoxifying Enzymes from Odontotermes formosanus (Shiraki) to the Stress Caused by Serratia marcescens Bizio (SM1)

Subterranean termite Odontotermes formosanus (Shiraki) (Blattodea: Isoptera: Termitidae), is a pest species found in forests and dams. Serratia marcescens Bizio (SM1) has a potential pathogenic effect on O. formosanus. However, the response of detoxifying enzymes to exposure by S. marcescens in O. formosanus has not been studied. In the present work, 20 detoxifying enzyme genes, including 6 glutathione S-transferases (GSTs), 5 UDP glycosyltransferases (UGTs) and 9 Cytochrome P450s (CYPs), were identified from the O. formosanus transcriptome dataset by bioinformatics analysis. Furthermore, the effects of SM1 infection on the transcription levels of detoxifying enzyme genes (GSTs, UGTs and CYPs) in O. formosanus were determined. The results showed that the expression of all detoxifying enzyme gene, except one GST, in O. formosanus were altered in response to the infection by SM1. The response of GSTs, UGTs and CYPs to SM1 in O. formosanus suggested that they may play an important role in the defense against bacterial infection such as SM1, and implies that termites have evolved a complex immune response to potential pathogens.

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

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.

Silencing Orco Impaired the Ability to Perceive Trail Pheromones and Affected Locomotion Behavior in Two Termite Species

Sophisticated social behaviors in termite colonies are mainly regulated via chemical communication of a wide range of pheromones. Trail pheromones play important roles in foraging behavior and building tunnels and nests in termites. However, it is almost unclear how termites perceive trail pheromones. Here, we cloned and sequenced of olfactory co-receptor (Orco) genes from the two termites Reticulitermes chinensis Snyder (Isoptera: Rhinotermitidae) and Odontotermes formosanus (Shiraki) (Isoptera: Termitidae), and then examined their responses to trail pheromones after silencing Orco through RNA interference (RNAi). We found that Orco knockdown impaired their ability to perceive trail pheromones and resulted in the disability of following pheromone trails in the two termite species. Our locomotion behavior assays further showed that Orco knockdown significantly decreased the distance and velocity in the two termite species, but significantly increased the angular velocity and turn angle in the termite R. chinensis. These findings strongly demonstrated that Orco is essential for termites to perceive their trail pheromones, which provides a potential way to control termite pests by damaging olfactory system.