Spatial and temporal anoxia in single-osculum Halichondria panicea demosponge explants studied with planar optodes

Abstract

AbstractThe 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 spatial and temporal anoxia in sponges is lacking, but important in elucidating interactions between sponge hosts and their microbiomes. 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 the demosponge Halichondria panicea. The present study reveals an intrinsic concentric deoxygenation pattern in explants during episodes of osculum contraction generating an oxygen gradient with increasing concentrations towards the explant periphery. Four sponge explants faced 25 episodes with substantial changes in internal oxygen and anoxia which prevailed for 4.4 h of the total 92.0 h observation period. The 2-D images revealed that the total area of the explant experiencing anoxia during periods of osculum contraction–expansion varied between 0.01 and 13.22% and was on average 7.4 ± 4.4% for all sponge explants. Furthermore, oxygen respiration, as approximated by the rate of change of oxygen concentration during deoxygenation of the explant interior, was similar throughout the oxic parts of the explant base. 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.