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Bely, A. E.

Publications and source records attributed to Bely, A. E..

3 recordsLinked to original sources

Injury improves tolerance to acute heat stress through induction of heat shock protein expression in the annelid Pristina leidyi

Evolutionary patterns of regeneration ability in animals may reflect the relative costs of injury versus regeneration on organismal function. While the cost of injury seems obvious, the investment of resources and other physiological effects produced by regeneration may be considerable, and the effects of both injury and regeneration may depend upon myriad factors intrinsic to organisms or within their environments. Such effects and how they vary are not well understood. We investigated the physiological effects of amputation injury and subsequent regeneration of tissue in the annelid Pristina leidyi, using environmental stress tolerance as a relevant measure of performance. Unexpectedly, injury improved survival under heat stress, but improved heat tolerance was unrelated to changes in metabolic rate. We performed TagSeq to investigate the transcriptional basis of injury-induced heat tolerance and found that injured worms produced an exaggerated response to subsequent heat stress compared to either injury or heat stress alone. Both injury and heat stress commonly induced the expression of just two heat shock family proteins. Pharmacological inhibition of one of these proteins, mortalin, drastically reduced heat tolerance in both uninjured and injured worms and substantially impaired anterior tissue regeneration. We posit that injury-induced expression of mortalin and other cellular stress response factors briefly confers improved resistance to broad forms of stress. Our work demonstrates that injury may have unpredictable effects and points to a shared ancestral response to various forms of biological damage with a critical role in animal function during the regeneration process.

physiology↗

Annelid adult cell type diversity and their pluripotent cellular origins

Annelids are a broadly distributed, highly diverse, economically and environmentally important group of animals. Most species can regenerate missing body parts, and many are able to reproduce asexually. Therefore, many annelids can generate all adult cell types in adult stages. However, the putative adult stem cell populations involved in these processes, as well as the diversity of adult cell types generated by them, are still unknown. Here, we recover 75,218 single cell transcriptomes of Pristina leidyi, a highly regenerative and asexually-reproducing freshwater annelid. We characterise all major annelid adult cell types, and validate many of our observations by HCR in situ hybridisation. Our results uncover complex patterns of regionally expressed genes in the annelid gut, as well as neuronal, muscle and epidermal specific genes. We also characterise annelid-specific cell types such as the chaetal sacs and globin+ cells, and novel cell types of enigmatic affinity, including a vigilin+ cell type, a lumbrokinase+ cell type, and a diverse set of metabolic cells. Moreover, we characterise transcription factors and gene networks that are expressed specifically in these populations. Finally, we uncover a broadly abundant cluster of putative stem cells with a pluripotent signature. This population expresses well-known stem cell markers such as vasa, piwi and nanos homologues, but also shows heterogeneous expression of differentiated cell markers and their transcription factors. In these piwi+ cells, we also find conserved expression of pluripotency regulators, including multiple chromatin remodelling and epigenetic factors. Finally, lineage reconstruction analyses reveal the existence of differentiation trajectories from piwi+ cells to diverse adult types. Our data reveal the cell type diversity of adult annelids for the first time and serve as a resource for studying annelid cell types and their evolution. On the other hand, our characterisation of a piwi+ cell population with a pluripotent stem cell signature will serve as a platform for the study of annelid stem cells and their role in regeneration.

genomics↗

A phylum-wide survey reveals multiple independent gains of head regeneration ability in Nemertea

Animals vary widely in their ability to regenerate, suggesting that regenerative abilities have a rich evolutionary history. However, our understanding of this history remains limited because regeneration ability has only been evaluated in a tiny fraction of species. Available comparative regeneration studies have identified losses of regenerative ability, yet clear documentation of gains is lacking. We surveyed regenerative ability in 34 species spanning the phylum Nemertea, assessing the ability to regenerate heads and tails either through our own experiments or from literature reports. Our sampling included representatives of the 10 most diverse families and all three orders comprising this phylum. We generated a phylogenetic framework using sequence data to reconstruct the evolutionary history of head and tail regeneration ability across the phylum and found that while all evaluated species can remake a posterior end, surprisingly few could regenerate a complete head. Our analysis reconstructs a nemertean ancestor unable to regenerate a head and indicates at least four separate lineages have independently gained head regeneration ability, one such gains reconstructed as taking place within the last 10-15 mya. Our study highlights nemerteans as a valuable group for studying evolution of regeneration and identifying mechanisms associated with repeated gains of regenerative ability.

evolutionary biology↗