An Efficient Antioxidant System in a Long-Lived Termite Queen

Abstract

The trade-off between reproduction and longevity is known in wide variety of animals. Social insect queens are rare organisms that can achieve a long lifespan without sacrificing fecundity. The extended longevity of social insect queens, which contradicts the trade-off, has attracted much attention because it implies the existence of an extraordinary anti-aging mechanism. Here, we show that queens of the termite Reticulitermes speratus incur significantly lower oxidative damage to DNA, protein and lipid and have higher activity of antioxidant enzymes than non-reproductive individuals (workers and soldiers). The levels of 8-hydroxy-2’-deoxyguanosine (oxidative damage marker of DNA) were lower in queens than in workers after UV irradiation. Queens also showed lower levels of protein carbonyls and malondialdehyde (oxidative damage markers of protein and lipid, respectively). The antioxidant enzymes of insects are generally composed of catalase (CAT) and peroxiredoxin (Prx). Queens showed more than two times higher CAT activity and more than seven times higher expression levels of the CAT gene RsCAT1 than workers. The CAT activity of termite queens was also markedly higher in comparison with other solitary insects and the queens of eusocial Hymenoptera. In addition, queens showed higher expression levels of the Prx gene RsPRX6. These results suggested that this efficient antioxidant system can partly explain why termite queens achieve long life. This study provides important insights into the evolutionary linkage of reproductive division of labor and the development of queens’ oxidative stress resistance in social insects.

Hypoxia adaptation in termites: hypoxic conditions enhance survival and reproductive activity in royals

“…In addition, vitellogenin is known to act as an antioxidant that promotes survival in honeybee queens (Seehuus et al ., ; Corona et al ., ). Antioxidant systems are thought to be associated with termite survival and also fecundity (Tasaki, Kobayashi et al ., ; Tasaki, Sakurai et al ., ). We found that, under hypoxic conditions, queens exhibited more than five times higher expression levels of RsCAT1 at 2 weeks than at 1 day (Fig.…”

“…A). As demonstrated in a previous study, a high level of RsCAT1 expression is a major characteristic of mature queens and may play an important role in the antioxidant system (Tasaki, Kobayashi et al ., ). On the other hand, kings exhibited more than twice the expression levels of RsPHGPX at 2 weeks than at 1 day under hypoxic conditions (Fig.…”

“…Using next‐generation RNA sequencing, the whole transcriptome of R. speratus was examined as described previously (Mitaka et al ., ). We used the messenger RNA sequence of the vitellogenin gene Vg1 and several antioxidant enzyme genes described in previous studies (Mitaka et al ., ; Tasaki, Kobayashi et al ., ). Since beta‐actin ( RsACT ) has been evaluated as the most reliable reference gene in Reticulitermes species, it was selected as the reference gene (Ishitani and Maekawa, ).…”

“…First, we compared the gene expression levels of vitellogenin – known as a yolk protein, contributing to the developing oocytes in queens – under hypoxic conditions and under control conditions, using quantitative real‐time PCR (qPCR) analysis. In addition to the vitellogenin gene expression analysis, we also compared several antioxidant enzyme genes reported as potentially being associated with fertility and longevity in the termite (Tasaki, Kobayashi et al ., ).…”

Economic and ecological importance of termites: A global review

“…The queens live 10–100 times longer than the workers (Tasaki et al . ,b). A termite queen can live up to 20 years (Makrushin ) and even 30 years (Keller ).…”