An Efficient Antioxidant System in a Long-Lived Termite Queen

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

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.

MeSH terms

  • 8-Hydroxy-2'-Deoxyguanosine
  • Animals
  • Antioxidants / metabolism*
  • Catalase / metabolism*
  • Deoxyguanosine / analogs & derivatives
  • Deoxyguanosine / metabolism
  • Female
  • Insect Proteins / metabolism*
  • Isoptera / metabolism*
  • Lipid Peroxidation / physiology
  • Longevity / physiology*
  • Peroxiredoxins / metabolism*

Substances

  • Antioxidants
  • Insect Proteins
  • 8-Hydroxy-2'-Deoxyguanosine
  • Peroxiredoxins
  • Catalase
  • Deoxyguanosine

Grants and funding

This work was supported by Japan Society for the Promotion of Science (https://www.jsps.go.jp/english/index.html, No. 26660113 to YI and No. 25221206 to KM).