Abstract

In most organisms, superoxide dismutases (SODs) are among the most effective antioxidant enzymes that regulate the reactive oxygen species (ROS) generated by oxidative energy metabolism. ROS are considered main proximate causes of aging. However, it remains unclear if SOD activities are associated with organismal longevity. The queens of eusocial insects, such as termites, ants, and honeybees, exhibit extraordinary longevity in comparison with the nonreproductive castes, such as workers. Therefore, the queens are promising candidates to study the underlying mechanisms of aging. Here, we found that queens have higher Cu/Zn-SOD activity than nonreproductive individuals of the termite Reticulitermes speratus. We identified three Cu/Zn-SOD sequences and one Mn-SOD sequence by RNA sequencing in R. speratus. Although the queens showed higher Cu/Zn-SOD activity than the nonreproductive individuals, there were no differences in their expression levels of the Cu/Zn-SOD genes RsSOD1 and RsSOD3A. Copper (Cu2+ and Cu+) is an essential cofactor for Cu/Zn-SOD enzyme activity, and the queens had higher concentrations of copper than the workers. These results suggest that the high Cu/Zn-SOD activity of termite queens is related to their high levels of the cofactor rather than gene expression. This study highlights that Cu/Zn-SOD activity contributes to extraordinary longevity in termites.

Highlights

  • Queens of termites, ants, and honeybees are representative eusocial insects that live up to 10 times longer than nonreproductive workers, they possess the same genome [1,2,3]

  • Via a subsequent homology search of the known amino acid sequence data from the termite Z. nevadensis and several model insects, we inferred the existence of three Cu/Zn-SOD sequences and one Mn-SOD sequence in the R. speratus transcriptome (Table S2)

  • By sequence alignments with the well-characterized SOD1 and SOD3 of Homo sapiens, Mus musculus, C. elegans, and D. melanogaster, that the R. speratus Cu/Zn-SODs had conserved all of the active sites that are essential for metal binding and disulphide formation [37], suggesting that they are active Cu/Zn-SODs (Figure 1)

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Summary

Introduction

Ants, and honeybees are representative eusocial insects that live up to 10 times longer than nonreproductive workers, they possess the same genome [1,2,3]. Caenorhabditis elegans (SOD5: NP 494779) GEIKGLSPG - - - - LHGFHIHQYGDSTDGCTSAGPHFNPCKMNHGGRDSVVRHVGD Drosophila melanogaster (SOD1: NP 476735) GEVCGLAKG - - - - LHGFHVHEFGDNTNGCMSSGPHFNPYGKEHGAPVDENRHLGD Zootermopsis nevadensis (SOD1: KDR12362) GEVTGLSQG - - - - LHGFHIHEFGDNTNGCISAGAHFNPHQKDHGSPTDEIRHVGD Reticulitermes speratus (RsSOD1: FX985484) GEVTGLSKG - - - - LHGFHIHEFGDNTNGCTSAGPHLNPYQKDHGGPGDEVRHLGD. Homo sapiens (SOD3: NP 003093) FALEGFPTEPNSSSRAIHVHQFGDLSQGCESTGPHYNPLAVPHP - - - - - - QHPGD Mus musculus (SOD3: NP 035565) FSLEGFPAEQNASNRAIHVHEFGDLSQGCDSTGPHYNPMEVPHP - - - - - - QHPGD Caenorhabditis elegans (SOD4: NP 001255003) GSVSGLAAG - - - - KHGFHIHEKGDTGNGCLSAGGHYNPHKLSHGAPDDSNRHIGD Drosophila melanogaster (SOD3: NP 725046) VQLEGLKEG - - - - KHGFHIHEKGDLTNGCIS MG AHYNPDKVDHGGPDHEVRHVGD Zootermopsis nevadensis (SOD3: KDR22972) ASIQGLRPPG - - - LHGFHLHRDGNTDNDCKAAGPHFNPFNHTHGGPDDAVRHAGD Reticulitermes speratus (RsSOD3A: FX985481) VSVQGLKPPG - - - LHGFHLHRDGNTDDDCKAAGPHFNPFNHTHGGPEDEFRHAGD Reticulitermes speratus (RsSOD3B: FX985482) GTVRGLIPGH - - - HHGFHVHEKGDIRNNCIAAGAHFNPENKNHGAPNDTERHVGD. We tested if the levels of SODs are higher in termite queens than in nonreproductive individuals

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