Molecular profiling of sponge deflation reveals an ancient relaxant-inflammatory response

Abstract

A hallmark of animals is the coordination of whole-body movement. Neurons and muscles are central to this, yet coordinated movements also exist in sponges that lack these cell types. Sponges are sessile animals with a complex canal system for filter-feeding. They undergo whole-body movements resembling “contractions” that lead to canal closure and water expulsion. Here, we combine 3D optical coherence microscopy, pharmacology, and functional proteomics to elucidate anatomy, molecular physiology, and control of these movements. We find them driven by the relaxation of actomyosin stress fibers in epithelial canal cells, which leads to whole-body deflation via collapse of the incurrent and expansion of the excurrent system, controlled by an Akt/NO/PKG/A pathway. A concomitant increase in reactive oxygen species and secretion of proteinases and cytokines indicate an inflammation-like state reminiscent of vascular endothelial cells experiencing oscillatory shear stress. This suggests an ancient relaxant-inflammatory response of perturbed fluid-carrying systems in animals.HighlightsSponge deflation is driven by tension release in actomyosin stress fibers of epithelial pinacocytesAkt kinase/Nitric oxide/Protein kinase G/A regulate actomyosin relaxationAgitation-induced deflation coincides with an inflammatory stateThe sponge relaxant-inflammatory response is evolutionary related to similar responses in the vertebrate vascular system