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

An Efficient Antioxidant System in a Long-Lived Termite Queen

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An Efficient Antioxidant System in a Long-Lived Termite Queen

Eisuke Tasaki et al. PLoS One. .
Free PMC article

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. The levels of oxidative damage are different between queens and non-reproductive workers in R. speratus.
Q, queens; W, workers. (A) The high caste polymorphism between queens and workers in eusocial termite R. speratus. Arrowheads indicate queens. (B) No difference in oxidative DNA damage was observed between queens and workers in control conditions (n = 6; for queen/worker: P = 0.106). However, after UV irradiation, queens showed lower levels of 8-OHdG than workers (n = 6; P < 0.001). (C) The levels of protein carboxyl were lower in the body of queens in comparison with workers in control conditions (n = 3; P = 0.019), as well as after UV irradiation (n = 3; P = 0.016). (D) Queens also had lower levels of oxidative lipid damage than workers in both control conditions (n = 3; P < 0.001) and UV irradiated conditions (n = 3; P < 0.001). We used pooled samples, shown as below (S1 Table), for each replication. White and black bars indicate control and post UV irradiation, respectively. Error bars represent standard error of the mean (SEM). Significance was measured using unpaired t test followed by Holm’s adjustment (NS, no significance; *P < 0.05, **P < 0.01).
Fig 2
Fig 2. Termite queens have high CAT activity and gene RsCAT1 expression.
A, adults; L, larvae; P, pupae; W, workers; M, male adults; Q, queens; S, soldiers; N, nymphs. (A) Queens of R. speratus (n = 12) had markedly higher CAT activity than D. melanogaster adults (n = 6; 10 individuals per replicate; P < 0.001), B. mori larvae (n = 6; P = 0.001), B. mori pupae (n = 6; P = 0.001), B. mori adults (n = 6; P < 0.001), T. aridifolia adults (n = 6; P < 0.001), C. obscuripes workers (n = 6; 5 individuals per replicate; P = 0.001), C. obscuripes queens (n = 3; P = 0.001), V. s. xanthoptera larvae (n = 3; P = 0.001), V. s. xanthoptera workers (n = 3; P = 0.001), V. s. xanthoptera adult males (n = 3; P = 0.001), V. s. xanthoptera queens (n = 3; P = 0.001), R. speratus workers (n = 6; P = 0.001), R. speratus soldiers (n = 6; P < 0.001), and R. speratus nymphs (n = 6; P = 0.001). The values of CAT activity in solitary insects were pooled male-female data (1:1). (B) Queens of R. speratus (n = 9) also showed higher CAT gene RsCAT1 expression than non-reproductive workers (n = 12; P < 0.001), soldiers (n = 12; P < 0.001), and nymphs (n = 12; P < 0.001). (C) There was no difference in CAT gene RsCAT2 expression between queens (n = 9) and non-reproductive individuals (n = 12; for queen/worker: P = 0.915; for queen/soldier: P = 0.915; for queen/nymph: P = 0.092). Except as specified in the text, we used one individual of solitary insects or eusocial Hymenoptera for several replications, whereas termite samples were pooled as described below (S1 Table). All data obtained between male and female of solitary insects and non-reproductive individuals of R. speratus were mixed by which the ratio of males and females was 1:1. Gray, white, and black bars indicate solitary insects, eusocial insects, and R. speratus queens, respectively. Error bars represent standard error of the mean (SEM). Significance was measured using unpaired t test followed by Holm’s adjustment (**P < 0.01).
Fig 3
Fig 3. Termite queens have high level of 1-Cys Prx gene RsPRX6 expression.
W, workers; S, soldiers; N, nymphs; Q, queens. (A) There was no difference in Prx activity between queens (n = 9) and non-reproductive individuals (n = 3; for queen/worker: P = 0.342; for queen/soldier: P = 0.279; for queen/nymph: P = 0.279). (B) Queens (n = 9) had higher levels of RsPRX6 gene expression than workers (n = 12; P < 0.001), soldiers (n = 12; P < 0.001), and nymphs (n = 12; P < 0.001). (C) Queens (n = 9) also had higher RsPRX1 gene expression than nymphs (n = 12; P = 0.002) but not workers (n = 12; P = 0.885) or soldiers (n = 12; P = 0.149). (D) The level of RsPRX4 gene expression in queens (n = 9) was also higher than nymphs (n = 12; P = 0.003) but not workers (n = 12; P = 0.184) or soldiers (n = 12; P = 0.236). (E) There was no difference in RsPRX5 gene expression between queens (n = 9) and non-reproductive individuals (n = 12; for queen/worker: P = 0.555; for queen/soldier: P = 0.555; for queen/nymph: P = 0.524). We used pooled samples for each replication, shown as below (S1 Table), for several replications. All data obtained between male and female of non-reproductive individuals were mixed by which the ratio of males and females was 1:1. White and black bars indicate non-reproductive individuals and queens, respectively. Error bars represent standard error of the mean (SEM). Significance was measured by unpaired t test followed by Holm’s adjustment (**P < 0.01)

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Grant support

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).
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