Contraction-Expansion and the Effects on the Aquiferous System in the Demosponge Halichondria panicea

Peter Funch,Josephine Goldstein,Nicklas Bisbo,Hans Ulrik Riisgård

doi:10.3389/fmars.2020.00113

Peter Funch, Josephine Goldstein + Show 2 more

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https://doi.org/10.3389/fmars.2020.00113

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Abstract

Contractile behavior is common among sponges despite their lack of nerves and muscles. As sessile filter-feeders, sponges rely on water with suspended food particles being pumped through their aquiferous system. During contractions, however, the water flow is being reduced and eventually shut down. Yet, purpose and underlying pathways of contractile behavior have remained largely unclear. Here we document the external and internal morphology of contracted and expanded single-osculum explants of the demosponge Halichondria panicea. We show that contraction-expansion dynamics can occur spontaneously (in untreated explants) and can be induced by exposure to chemical messengers such as -aminobutyric acid (GABA, 1 mM) and L-glutamate (L-Glu, 1 mM), or to inedible ink particles (4 mg L-1). The neurotransmitter GABA triggered similar contraction-expansion dynamics in H. panicea as observed in untreated explants. The effects of GABA-induced contraction-expansion events on the aquiferous system were investigated using scanning electron microscopy (SEM) on cryofractured explants. Our findings suggest that contraction-expansion affects the entire aquiferous system of H. panicea, including osculum, ostia, in- and excurrent canals and apopyles.

Highlights

Sponges are sessile filter-feeders that pump water by means of choanocytes (Reiswig, 1975; Asadzadeh et al, 2019) which are specialized flagellated cells that efficiently retain particles down to ∼0.1 μm on their microvilli collars (Riisgård and Larsen, 2000)
Ambient water is drawn through numerous inhalant openings into an incurrent canal system, where it enters many choanocyte chambers (CCs) through prosopyles, passes microvillar collar-sieves, exits the CC through apopyles and leaves the sponge via an excurrent canal system that leads to an exhalant opening, the osculum (Larsen and Riisgård, 1994)
Signaling in demosponges is poorly understood but probably involves non-motile primary sensory cilia (Nickel, 2010; Ludeman et al, 2014; Leys, 2015), conduction pathways based on chemical messengers (Ellwanger and Nickel, 2006; Ellwanger et al, 2007) and an antagonistic contractile apparatus, most likely mediated by the pinacoderm as effector and the water pressure generated by the choanocytes (Nickel et al, 2011)

Summary

INTRODUCTION

Sponges are sessile filter-feeders that pump water by means of choanocytes (Reiswig, 1975; Asadzadeh et al, 2019) which are specialized flagellated cells that efficiently retain particles down to ∼0.1 μm on their microvilli collars (Riisgård and Larsen, 2000). We determine the trigger potential of neurotransmitters and inedible particles compared to spontaneous (untreated conditions) contractionexpansion events in single-osculum explants of H. panicea We use these findings to induce similar contractionexpansion events as observed in untreated explants and study the resulting effects on the aquiferous system in explants fixed in different contraction-expansion phases using scanning electron microscopy (SEM). Using GLMMs with Gamma error structure, we compared the rates of contraction/expansion, duration of the contracted phase in OSA or A, and the volume change during contraction/expansion, respectively, after exposure to different treatments (GABA, L-Glu or inedible particles; fixed effect) to spontaneous (untreated) contraction-expansion dynamics by taking into account variable A (fixed effect) and individual variation of explants (ID#; random effect). Similar GLMMs were parameterized to investigate changes in the diameter (D) of ostia, canals and apopyles during different contractile phases of explants (fixed effect) by correcting for individual variation (ID#; random effect)

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