Oxygen regulation in the earliest animals: spatiotemporal resolution of oxygen dynamics in single-osculum Halichondria panicea and Haliclona rosea sponges.

Sponges regulate internal water flow and oxygen distribution through contractile behavior, yet the mechanisms governing spatio-temporal oxygen dynamics remain poorly understood. Resolving these dynamics in sponges is crucial for understanding sponge host-microbiome interactions, tissue homeostasis and growth. We applied 2-D luminescence lifetime imaging of oxygen to unveil temporal as well as spatial oxygen dynamics in single-osculum explants of two demosponges: Halichondria panicea and Haliclona rosea. Our study reveals intrinsic deoxygenation in explants during episodes of osculum contraction generating an oxygen gradient with increasing concentrations towards the explant periphery. Furthermore, time-lapse oxygen imaging uncovered contrasting spatio-temporal patterns of internal O2 distribution in the examined individuals of the two species. Four explants of H. panicea faced periodic and consistent episodes of internal oxygen drawdowns and centralized anoxia, followed by reoxygenation. Periods of internal anoxia persisted for up to 4.5 h of the total 92.1-hour observation period. Conversely, two H. rosea explants displayed versatile deoxygenation patterns, including recurring, propagating waves of oxygen reduction, with relatively few areas experiencing anoxia over the course of the 70.6-hour observation period. The observed oxygen dynamics indicate that filter-feeding sponges may employ distinct behavior to actively regulate their internal oxygenation. We suggest that spatiotemporal oxygen regulation may represent an ancestral trait that emerged in early diverging metazoans, and possibly in response to increasing levels of atmospheric oxygen.