Long-lived termite kings and queens activate telomerase in somatic organs
Kings and queens of termites, like reproductive individuals of other advanced eusocial insects, are endowed with admirable longevity, which dramatically exceeds the life expectancies of their non-reproducing nest-mates and related solitary insects. In this study, we tested the possible correlation between the activation of the telomerase mechanism and differential longevities of termite castes.
Figure 1. Telomerase catalytic activity, identification of telomeric repeats and telomere lengths in P. simplex. (a) Electrophoretic separation of TRAP products. (b) FISH of (TTAGG)n-specific probe with metaphase nuclear preparation. (c) Terminal restriction fragment (TRF) analysis of somatic genomic DNA (gDNA) from different castes. (d ) TRF analysis of somatic gDNA from two different worker stages.
In the quest to find the mechanisms underlying the longevity of termite reproductives, we focused on somatic maintenance mediated by telomerase. This ribonucleoprotein is well established for pro-longevity functions in vertebrates, thanks primarily to its ability of telomere extension. However, its participation in lifespan regulation of insects, including the eusocial taxa, remains understudied.
In this study, we tested the possible correlation between the activation of the telomerase mechanism and differential longevities of termite castes. In our main model, P. simplex, we characterized the gene and protein structure of TERT (the catalytic subunit of telomerase), including transcript and protein variants, quantified TERT transcript and protein abundances, telomerase activities and lengths of telomeres across different castes, life stages and organs, with emphasis on the differences between reproductives and workers, from which the reproductives develop.
We demonstrated a strong association between the life expectancies of different castes and the somatic activation of telomerase. In the soma of long-lived primary and neotenic kings and queens of P. simplex, we observed a conspicuous increase in telomerase catalytic activity (Figure 1a) and quantity of the TERT protein when compared with workers. We confirmed the main finding on the somatic telomerase activation also in the reproductives of two other species with different caste systems and developmental patterns. Telomerase activation also took place in tissues, which are expected to have low mitotic activity, like the ventral nerve cord. These results contrast with the conventional view of telomerase, whose activity should be low or absent in adult somatic organs with low proliferative potential.
In parallel, we studied the lengths of telomeres in P. simplex and two other termites (Figure 1c, d). The telomeres in all phenotypes and species were relatively long (up to over 50 kb) and did not show length differences that might explain the differential longevity or observed differences in telomerase activities and abundances. We conclude that although our observations are inline with the broadly assumed association between telomerase and longevity, the potential prolongevity mechanism of telomerase in reproductives remains elusive.
Koubová J., Pangrácová M., Jankásek M., Lukšan O., Jehlík T., Brabcová J., Jedlička P., Křivánek J., Čapková Frydrychová R., Hanus R. (2021) Long-lived termite kings and queens activate telomerase in somatic organs. Proceedings of the Royal Society B 288: 20210511. doi: 10.1098/rspb.2021.0511.