Gene expression and co-expression heterogeneity patterns during the cell cycle and biodemography analyses encourage aging studies in archaea

Some prokaryotic ancestors of eukaryotes were archaea, but do these cells age, and if so, how? Uncovering aging in Archaea might provide more general clues about cellular senescence and rejuvenation and their origins. To fill this knowledge gap, we focused on Saccharolobus islandicus, a model archaeon for which the cell cycle can be synchronized and controlled. We generated longitudinal transcriptomes of synchronized S. islandicus populations that capture typical expression and co-expression profiles associated with chronological aging. These experiments also allowed us to infer average cellular death rates during the cell cycle. Our results are compatible with general patterns of biological aging observed in single cells. However, at the population level we observe a peak of mortality shortly after cell division in S. islandicus, which we interpret as "negative" demographic aging or ontogenescence, i.e., pre-reproductive mortality decline. To reconcile these observations, we propose a model of S. islandicus aging and rejuvenation. Our research constitutes a first step into the study of aging in archaea on the basis of gene expression, gene co-expression patterns during the cell cycle and biodemography analyses, and to propose a hypothetical new model to explore how cellular senescence and rejuvenation in eukaryotes may have prokaryotic roots. Alternative interpretations of our transcriptomic results however are possible, encouraging future experimental validation of aging in Archaea.