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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.
Highlights
Tissue homeostasis is the capacity to maintain, via feedback loops, the internal conditions that allow the proper functioning of an animal
We focused our attention on marine sponges (Phylum Porifera) because they play a key role in the e cosystem[24,25,26], they belong to the group of animals with high regenerative capacity[27], and constitute one of the earliest-diverging animal lineages[28,29]; but, compared to other animal groups, they have been little s tudied[30]
We found eight genes defined as key regulators of ancient gene networks by Trigos et al 58; three of them appeared as hubs in the A. queenslandica-based network (i.e., Dvl, Tcf, and MAPK3) (Fig. 5)
Summary
Tissue homeostasis is the capacity to maintain, via feedback loops, the internal conditions that allow the proper functioning of an animal. For understanding the mechanisms of tissue repair[9,12,13,14,15] and recent studies suggest that they may share common molecular features at the early points of r egeneration[16,17], at the time of the recognition and signaling of the wound[16,18,19]. Beyond these classical model systems, we know very little about the molecular mechanisms involved in animal response to wounding.
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