Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite

Abstract

Eusocial termite queens achieve nearly maximal fertility throughout their extremely long life without apparent signs of aging. Termites represent, therefore, an ideal model for aging research. To investigate the molecular mechanisms underlying their long reproductive life, we carried out transcriptomic, lipidomic and metabolomic analyses on fat bodies of sterile short lived workers, long-lived kings and five stages spanning twenty years of adult queen maturation. In mature reproductives, genes supporting a robust mitochondrial functioning or associated with genome stability were upregulated. In most organisms, insulin signaling increases fertility but decreases lifespan, often accompanied by harmful lipid signatures. Our findings suggest that an upregulation of insulin-like peptide (Ilp9) in the fat body of termite queens is accompanied by a specific lipid metabolism, limiting fat storage, thus sustaining both high fertility and maintaining extreme lifespan. Our results highlight potential molecular targets for research into aging-related metabolic diseases linked to the accumulation of excess fat.

Complex regulatory role of DNA methylation in caste- and age-specific expression of a termite

“…This pipeline involves first formatting the gff and then extracting exon read counts from sam files. These sam files had been created in a previous study These termites were collected from field colonies (colony ID) in 2016 in Southern Africa as described in (Séité et al, 2022). The number of individuals pooled per sample, the bisulfite non-conversion rates, total numbers of sequenced reads, and mapping rates are indicated.…”

“…Additionally, we assembled a genome-guided transcriptome from RNAseq data (accessions: SAMN17088123-SAMN17088147) (Séité et al, 2022), using the new tuxedo protocol (Pertea et al, 2016). Raw reads were trimmed using Trimmomatic (v0.38) (Bolger et al, 2014) with parameters TRAILING:25 LEADING:25 SLIDINGWINDOW:4:20 AVGQUAL:20 MINLEN:50.…”

“…Genes containing significantly differentially methylated sites between young, virgin queens and mature queens.Dmel & Hsap: ortholog in Drosophila melanogaster and Homo sapiens. DE: differential expression between VQ & MQ(Séité et al, 2022).…”

“…This table contains the origin of the fat body obtained from the 4 Macrotermes natalensis phenotypes (female worker, FW; virgin queens, VQ; mature queens, MQ; mature kings, MK) analysed in this study. These termites were collected from field colonies (colony ID) in 2016 in Southern Africa as described in (Séité et al, 2022). The number of individuals pooled per sample, the bisulfite non-conversion rates, total numbers of sequenced reads, and mapping rates are indicated.…”

“…Dmel & Hsap: ortholog in Drosophila melanogaster and Homo sapiens. DE: differential expression between VQ & MQ(Séité et al, 2022).…”