Wounding response in Porifera (sponges) activates ancestral signaling cascades involved in animal healing, regeneration, and cancer

Abstract

Abstract Upon injury, the homeostatic balance that ensures tissue function is disrupted. Wound-induced signaling triggers the recovery of tissue integrity and offers a context to understand the molecular mechanisms for restoring tissue homeostasis upon disturbances. Marine sessile animals are particularly vulnerable to chronic wounds caused by grazers that can compromise prey’s health. Yet, in comparison to other stressors like warming or acidification, we know little on how marine animals respond to grazing. Marine sponges (Phylum Porifera) are among the earliest-diverging animals and play key roles in the ecosystem; but they remain largely understudied. Here, we investigated the transcriptomic responses to injury caused by a specialist spongivorous opisthobranch (i.e., grazing treatment) or by clipping with a scalpel (i.e., mechanical damage treatment), in comparison to control sponges. We collected samples 3 h, 1 d, and 6 d post-treatment for differential gene expression analysis on RNA-seq data. Both grazing and mechanical damage activated a similar transcriptomic response, including a clotting-like cascade (e.g., with genes annotated as transglutaminases, metalloproteases, and integrins), calcium signaling, and Wnt and mitogen-activated protein kinase signaling pathways. Wound-induced gene expression signature in sponges resembles the initial steps of whole-body regeneration in other animals. Also, the set of genes responding to wounding in sponges included putative orthologs of cancer-related human genes. Further insights can be gained from taking sponge wound healing as an experimental system to understand how ancient genes and regulatory networks determine healthy animal tissues.