Nejvíce citovaný článek - PubMed ID 33878922
Long-lived termite kings and queens activate telomerase in somatic organs
Pheromone communication is the cornerstone of eusocial insect societies since it mediates the social hierarchy, division of labor, and concerted activities of colony members. The current knowledge on molecular mechanisms of social insect pheromone detection by odorant receptors (ORs) is limited to bees and ants, while no OR was yet functionally characterized in termites, the oldest eusocial insect clade. Here, we present the first OR deorphanization in termites. We selected four OR sequences from the annotated antennal transcriptome of the termite Prorhinotermes simplex (Psammotermitidae), expressed them in Empty Neuron Drosophila, and functionally characterized them using single sensillum recording (SSR). For one of the selected ORs, PsimOR14, we obtained strong responses to the main component of P. simplex trail-following pheromone, the monocyclic diterpene neocembrene. PsimOR14 showed a narrow tuning to neocembrene with only one additional compound out of 67 tested generating non-negligible responses. We report on homology-based modeling and molecular dynamics simulations of ligand binding by PsimOR14. Subsequently, we used SSR in P. simplex workers and identified the olfactory sensillum responding to neocembrene, thus likely expressing PsimOR14. Finally, we demonstrate that PsimOR14 is significantly more expressed in worker antennae compared to soldiers, which correlates with higher sensitivity of workers to neocembrene.
- Klíčová slova
- D. melanogaster, Prorhinotermes simplex, deorphanization, neuroscience, odorant receptor, pheromone receptor, termite, trail-following pheromone,
- MeSH
- feromony metabolismus MeSH
- hmyzí proteiny * metabolismus genetika MeSH
- Isoptera * genetika fyziologie metabolismus MeSH
- receptory pachové * metabolismus genetika MeSH
- receptory pro feromony * metabolismus genetika chemie MeSH
- sensilla fyziologie MeSH
- tykadla členovců metabolismus MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- feromony MeSH
- hmyzí proteiny * MeSH
- receptory pachové * MeSH
- receptory pro feromony * MeSH
Kings and queens of termites are endowed with an extraordinary longevity coupled with lifelong fecundity. We recently reported that termite kings and queens display a dramatically increased enzymatic activity and abundance of telomerase in their somatic organs when compared to short-lived workers and soldiers. We hypothesized that this telomerase activation may represent a noncanonical pro-longevity function, independent of its canonical role in telomere maintenance. Here, we explore this avenue and investigate whether the presumed noncanonical role of telomerase may be due to alternative splicing of the catalytic telomerase subunit TERT and whether the subcellular localization of TERT isoforms differs among organs and castes in the termite Prorhinotermes simplex. We empirically confirm the expression of four in silico predicted splice variants (psTERT1-A, psTERT1-B, psTERT2-A, psTERT2-B), defined by N-terminal splicing implicating differential localizations, and C-terminal splicing giving rise to full-length and truncated isoforms. We show that the transcript proportions of the psTERT are caste- and tissue-specific and that the extranuclear full-length isoform TERT1-A is relatively enriched in the soma of neotenic kings and queens compared to their gonads and to the soma of workers. We also show that extranuclear TERT protein quantities are significantly higher in the soma of kings and queens compared to workers, namely due to the cytosolic TERT. Independently, we confirm by microscopy the extranuclear TERT localization in somatic organs. We conclude that the presumed pleiotropic action of telomerase combining the canonical nuclear role in telomere maintenance with extranuclear functions is driven by complex TERT splicing.
- Klíčová slova
- Isoptera, TERT, alternative splicing, longevity, telomerase, termites,
- MeSH
- alternativní sestřih MeSH
- dlouhověkost * MeSH
- hmyzí proteiny * metabolismus genetika MeSH
- Isoptera * fyziologie enzymologie genetika MeSH
- protein - isoformy metabolismus genetika MeSH
- telomerasa * metabolismus genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- hmyzí proteiny * MeSH
- protein - isoformy MeSH
- telomerasa * MeSH
Studies on human telomeres have established that telomeres exert a significant influence on lifespan and health of organisms. However, recent research has indicated that the original idea that telomeres affect lifespan in a universal and central manner across all eukaryotic species is an oversimplification. Indeed, findings from a variety of animal species revealed that the role of telomere biology in aging is more subtle and intricate than previously recognized. Here, we show how telomere biology varies depending on the taxon. We also show how telomere biology corresponds to basic life history traits and affects the life table of a species and investments in growth, body size, reproduction, and lifespan; telomeres are hypothesized to shape evolutionary perspectives for species in an active but complex manner. Our evaluation is based on telomere biology data from many examples from throughout the animal kingdom that vary according to the degree of organismal complexity and life history strategies.
- Klíčová slova
- Aging, Life history traits, Lifespan, Telomerase, Telomeres,
- MeSH
- biologická evoluce MeSH
- dlouhověkost MeSH
- lidé MeSH
- stárnutí genetika MeSH
- telomerasa * genetika MeSH
- telomery MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- telomerasa * MeSH
Termites are dominant animals of tropical terrestrial ecosystems. Their success is due to their eusocial organization as well as their ability to digest dead plant tissues. While being extremely abundant, the termite diet is poor in crucial nutrients, such as fatty acids. Linoleic acid (LA) is a precursor for many vital biomolecules, and most animals depend on its dietary supply. Termites count among the exceptions known to produce LA de novo, presumably via the action of an unknown Δ12 fatty acyl desaturase (FAD) introducing the second double bond into monounsaturated oleic acid. Here, we search for the evolutionary origin of LA biosynthesis in termites. To this end, we compile the repertoire of FAD homologs from 57 species of termites and their closest relatives, the cockroaches, analyze FAD phylogeny, and identify a potential Δ12 FAD branch, which arose through duplication of a likely Δ9 FAD. We functionally characterize both paralogs and identify the Δ9 activity in the ancestral FAD-A1a and the Δ12 activity responsible for LA biosynthesis in FAD-A1b. Through the combination of homology modeling and site-directed mutagenesis, we pinpoint structural features possibly contributing to the distinct functions, regiospecificities, and substrate preferences of the two enzymes. We confirm the presence of both paralogs in all 36 studied species of the Blattoidea lineage (Blattidae, Lamproblattidae, Cryptocercidae, and termites) and conclude that we identified an evolutionary event important for the ecological success of termites, which took place in their cockroach ancestors roughly 160 My and remained conserved throughout termite diversification into 3,000 extant species.
- Klíčová slova
- Blattodea, Isoptera, biosynthesis, fatty acyl desaturases, linoleic acid, termites,
- MeSH
- ekosystém MeSH
- fylogeneze MeSH
- Isoptera * genetika MeSH
- kyselina linolová MeSH
- mastné kyseliny MeSH
- švábi * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- kyselina linolová MeSH
- mastné kyseliny MeSH