Spatio-temporal resolution of oxygen dynamics in single-osculum Halichondria panicea and Haliclona rosea explants

The water flow through sponges is regulated by their contractile behaviour including contraction and expansion of the aquiferous system, which leads to shifting oxygen levels in the sponge interior. Still, knowledge of internal oxygen dynamics in sponges is lacking, but important in elucidating sponge host-microbiome interactions, tissue homeostasis and growth. We combined 2-D luminescence lifetime imaging of oxygen with simultaneous time-lapse recordings of the sponge exhalant opening (osculum) to unveil temporal as well as spatial oxygen dynamics caused by contractile behaviour in single-osculum explants of two demosponges, Halichondria panicea and Haliclona rosea. The present study shows intrinsic deoxygenation in explants during episodes of osculum contraction generating an oxygen gradient with increasing concentrations towards the explant periphery. Furthermore, time-lapse oxygen images revealed distinctive spatio-temporal patterns for the internal distribution of O₂ in explants of different species. Explants of H. panicea faced consistent episodes with substantial changes in internal oxygen and centralized anoxia which prevailed for up to 4.4 h of the total 92 h observation period. In H. rosea explants, oxygen images displayed versatile deoxygenation patterns, such as recurring, propagating waves of oxygen reduction, with relatively few areas experiencing anoxia over the course of the 70-hour observation period. The resolved 2-D dynamics provide an unprecedented insight into the internal O₂ distribution of sponges and complement the traditional point measurements of oxygen sensors.