PLoS One. 2017 Jan 11;12(1):e0167412. doi: 10.1371/journal.pone.0167412.

An Efficient Antioxidant System in a Long-Lived Termite Queen.

Tasaki E1,2, Kobayashi K3, Matsuura K3, Iuchi Y1,2,4.
1Department of Applied Bioresources Chemistry, The United Graduate School of Agriculture, Tottori University, Tottori, Japan.
2Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Japan.
3Department of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.
4Graduate School of Sciences and Technology for Innovation, Yamaguchi University, Yamaguchi, Japan.

 

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.

PMID: 28076409

Supplement:

This study suggests that an efficient antioxidant system contributes to the long life of termite queens. Significantly lower oxidative damages to biomolecules such as DNA, proteins, and lipids were exhibited by termite queens than by non-reproductive workers. Moreover, a higher catalase (CAT) activity and higher CAT and 1Cys peroxiredoxin (Prx) gene expressions were observed in termite queens than in non-reproductive termites (workers and soldiers). CAT and Prx efficiently convert hydrogen peroxide (H2O2), a major reactive oxygen species (ROS). A superoxide anion and H2O2 can result in a hydroxyl radical that is generally considered to be one of the most toxic ROS. Because no study has discovered an enzyme that detoxifies a hydroxyl radical in organisms, CAT and Prx are considered to be important checkpoints in termite queens. However, avoiding hydroxyl radical formation is impossible. Therefore, a non-enzymatic system that comprises chemicals such ascorbic acid and polyphenols neutralized the deleterious radicals in most organisms. We previously demonstrated that non-reproductive termites use large quantities of uric acid as an antioxidant [1]. Although uric acid is the end product of purine degradation in insects, non-reproductive termites use it as an effective antioxidant. Interestingly, a higher radical scavenging activity was not exhibited by termite queens than by non-reproductive termites, suggesting the existence of different antioxidant systems in termite queens and non-reproductive termites (Figure 1).

 

Figure 1. Scheme of the antioxidant system in termite queens and non-reproductive termites.

 

Reference

  1. Tasaki E, Sakurai H, Nitao M, Matsuura K, Iuchi Y, Ohkuma M. Uric acid, an important antioxidant contributing to survival in termites. PLoS One. 2017;12: e0179426. doi:10.1371/journal.pone.0179426