ATP and glutamate coordinate contractions in the freshwater sponge Ephydatia muelleri
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Abstract
Sponges (phylum Porifera ) are an early diverging animal lineage that lacks both conventional nervous and muscular systems, and yet they are able to produce coordinated whole-body contractions in response to disturbances. Little is known about the underlying signaling mechanisms in coordinating such responses. Previous studies demonstrated that sponges respond specifically to neuroactive chemicals such as L-glutamate and γ-amino-butyric acid (GABA), which trigger and prevent contractions respectively. Genes for purinergic P2X-like receptors are present in several sponge genomes, leading us to ask whether ATP works with glutamate to coordinate contractions in sponges as it does in other animal nervous systems. Using pharmacological approaches on the freshwater sponge Ephydatia muelleri , we show that ATP is involved in coordinating contractions. Bath applications of ATP cause a rapid, sustained expansion of the excurrent canals in a dose-dependent manner. Complete contractions occur when ATP is added in the presence of apyrase, an enzyme that hydrolyzes ATP. Applying ADP, the first metabolic product of ATP hydrolysis, triggers complete contractions, whereas AMP, the subsequent metabolite, does not trigger a response. Blocking ATP from binding and activating P2X receptors with pyridoxalphosphate-6-azophenyl-2’,4’-disulfonic acid (PPADS) prevents both glutamate- and ATP-triggered contractions, suggesting that ATP works downstream of glutamate. Bioinformatic analysis revealed two P2X receptor sequences, one which groups with other vertebrate P2X receptors. Altogether, our results confirm that purinergic signaling by ATP is involved in coordinating contractions in the freshwater sponge suggesting a role of ATP-mediated signaling that predates the evolution of the nervous system and multicellularity in animals.
Summary statement
Nerveless sponges coordinate a sneeze-like reflex using glutamate and ATP signaling to expel water from the body.
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Glutamate signaling in astrocytes causes the release of ATP which stimulates propagation of Ca2+ signals (Hamilton et al., 2008). We propose that a similar pathway regulates contraction behaviours in sponges as described in Fig. 5.
Congrats on the fascinating paper on an organism without a conventional nervous system. I'm interested in the functional analogies you propose to astrocytes (vs neurons) based on the described ATP and glutamate dynamics you describe. Do you think that a comparative approach in terms of other features of nervous system cells—expression profiles, cell morphological features and connectivity (i.e. gap junctions)—would be useful for distinguishing and understanding the function of these sponge cells? Or help us think about how nervous system cells like neurons and astrocytes became more specialized in animals …
Glutamate signaling in astrocytes causes the release of ATP which stimulates propagation of Ca2+ signals (Hamilton et al., 2008). We propose that a similar pathway regulates contraction behaviours in sponges as described in Fig. 5.
Congrats on the fascinating paper on an organism without a conventional nervous system. I'm interested in the functional analogies you propose to astrocytes (vs neurons) based on the described ATP and glutamate dynamics you describe. Do you think that a comparative approach in terms of other features of nervous system cells—expression profiles, cell morphological features and connectivity (i.e. gap junctions)—would be useful for distinguishing and understanding the function of these sponge cells? Or help us think about how nervous system cells like neurons and astrocytes became more specialized in animals with conventional nervous systems?
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