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

Morten Larsen,Ronnie N. Glud,Donald E. Canfield,Lars Kumala

doi:10.1007/s00227-021-03980-2

Morten Larsen, Ronnie N. Glud + Show 2 more

Open Access

https://doi.org/10.1007/s00227-021-03980-2

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Abstract

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 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.

Highlights

Sponges are sedentary filter-feeding invertebrates that are characterized by a ‘simple’ body plan designed to obtain suspended food particles and oxygen by active waterpumping
Diffusive flux of oxygen across the exopinacoderm (Kumala and Canfield 2018). They lack true organs, muscles (Pavans de Cecatty 1986, 1989) and a nervous system (Jones 1962; Pavans de Cecatty 1974). Such contractile behaviour is coordinated by actin microfilaments, myocytes and actinocytes abundantly located in the pinacoderm, canal system and the exhalant opening known as the osculum (Prosser et al 1962; Elliott and Leys 2007; Nickel et al 2011)
Oxygen measured at the base of single-osculum Halichondria panicea explants (n = 4, ID1-4) approached the levels in the ambient seawater for most, i.e. 78 ± 3% of the total observation period of 92 h (Fig. 2)

Summary

Introduction

Sponges are sedentary filter-feeding invertebrates that are characterized by a ‘simple’ body plan designed to obtain suspended food particles and oxygen by active waterpumping. They lack true organs, muscles (Pavans de Cecatty 1986, 1989) and a nervous system (Jones 1962; Pavans de Cecatty 1974) Such contractile behaviour is coordinated by actin microfilaments, myocytes and actinocytes abundantly located in the pinacoderm, canal system and the exhalant opening known as the osculum (Prosser et al 1962; Elliott and Leys 2007; Nickel et al 2011). The diminished oxygen supply during pumping cessation may change the redox state of the sponge interior (Kumala and Canfield 2018), which is colonized by highly diverse microbial consortia (e.g. Taylor et al 2007; Thomas et al 2016; Moitinho-Silva et al 2017; Lurgi et al 2019)

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Conclusion