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Long-lived termite kings and queens activate telomerase in somatic organs.

ABSTRACT: Kings and queens of termites, like queens 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 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. Here, we report a conspicuous increase of telomerase abundance and catalytic activity in the somatic organs of primary and secondary reproductives of the termite Prorhinotermes simplex and confirm a similar pattern in two other termite species. These observations stand in contrast with the telomerase downregulation characteristic for most adult somatic tissues in vertebrates and also in solitary insects and non-reproducing castes of termites. At the same time, we did not observe caste-specific differences in telomere lengths that might explain the differential longevity of termite castes. We conclude that although the telomerase activation in termite reproductives is in line with the broadly assumed association between telomerase and longevity, its direct phenotypic impact remains to be elucidated.

SUBMITTER: Koubova J

PROVIDER: S-EPMC8059557 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundMost insects are relatively short-lived, with a maximum lifespan of a few weeks, like the aging model organism, the fruit-fly Drosophila melanogaster. By contrast, the queens of many social insects (termites, ants and some bees) can live from a few years to decades. This makes social insects promising models in aging research providing insights into how a long reproductive life can be achieved. Yet, aging studies on social insect reproductives are hampered by a lack of quantitative data on age-dependent survival and time series analyses that cover the whole lifespan of such long-lived individuals. We studied aging in queens of the drywood termite Cryptotermes secundus by determining survival probabilities over a period of 15 years and performed transcriptome analyses for queens of known age that covered their whole lifespan.ResultsThe maximum lifespan of C. secundus queens was 13 years, with a median maximum longevity of 11.0 years. Time course and co-expression network analyses of gene expression patterns over time indicated a non-gradual aging pattern. It was characterized by networks of genes that became differentially expressed only late in life, namely after ten years, which associates well with the median maximum lifespan for queens. These old-age gene networks reflect processes of physiological upheaval. We detected strong signs of stress, decline, defense and repair at the transcriptional level of epigenetic control as well as at the post-transcriptional level with changes in transposable element activity and the proteostasis network. The latter depicts an upregulation of protein degradation, together with protein synthesis and protein folding, processes which are often down-regulated in old animals. The simultaneous upregulation of protein synthesis and autophagy is indicative of a stress-response mediated by the transcription factor cnc, a homolog of human nrf genes.ConclusionsOur results show non-linear senescence with a rather sudden physiological upheaval at old-age. Most importantly, they point to a re-wiring in the proteostasis network and stress as part of the aging process of social insect queens, shortly before queens die.

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Long-lived termite kings and queens activate telomerase in somatic organs.

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