Cytoskeletal architecture, organelle transport, and impulse conduction in hexactinellid sponge syncytia

Date

2017-05-15

Authors

Leys, Sally Penelope

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Abstract

Hexactinellid sponges differ substantially from other sponges in having syncytial tissues and the ability to propagate signals rapidly, causing the arrest of the feeding current. To confirm existing light and electron microscopic evidence of the syncytial nature of hexactinellid tissue, live tissue models were developed from Rhabdocalyptus dawsoni and Aphrocallistes vastus. A native acellular tissue extract (ATE) was made from the sponges to which dissociated tissue adhered and spread in a species specific fashion. Video microscopy shows that dissociated tissue from R. dawsoni adheres to the ATE and aggregates by fusion of pieces to form a giant, multinucleated syncytium. Fusion, corroborated by dye exchange, is characterized by the bidirectional transport of organelles, including nuclei, and bulk cytoplasm at an average rate of 2.1 um·S⁻¹. Stress fibres line the periphery of adherent preparations, and giant actindense filopodia appear to anchor tissue to the substrate. Bundles of microtubules (MTs) bridge newly fused aggregates while extensive tracts of MT bundles are oriented in all directions in larger aggregates. Aggregates can become several centimetres in diameter and can cover a 5 cm² petri dish within 6-12 hours. Inhibition of organelle motility by colcemid and nocodazole but not by cytochalasin B suggests that transport occurs along MT bundles. A protein immunoreactive with cytoplasmic dynein was identified in whole cell lysate from A. vastus, and it is suspected the same motor protein exists in R. dawsoni and other hexactinellids. No evidence was found for kinesin, although its presence cannot be ruled out. Ultrastructural evidence suggests that a membranous network may be involved in linking bulk cytoplasm to bundles of microtubules in streams, in a manner similar to the mechanism by which bulk cytoplasm is linked to microfilaments in characean algae. Transport of bulk cytoplasm and movement of individual organelles can also be seen in regenerating fragments of the whole sponge suggesting that cytoplasmic streaming may be involved in tissue morphogenesis. The fact that latex beads that are phagocytosed are also transported in streams indicates that hexactinellid sponges employ symplastic nutrient transport, like plants, rather than apoplastic nutrient transport, like animals. Because fusion and cytoplasmic streaming are features of both Rhabdocalyptus and Aphrocallistes, representatives of lysaccine and dictyonal hexactinellids respectively, it is probable that these phenomena are characteristic of the subphylum Symplasma. Propagated arrests of the feeding current were recorded from Rhabdocalyptus in response to an increase in sediment in the sea water. Development of a new preparation in which aggregates are grafted on to parts of the adult body wall that demonstrate normal pumping physiology, allowed recording of action potentials which propagate through the sponge at 0.18 cm·s⁻¹, simultaneously with the arrest of the feeding current. This is the first recording of a propagated electrical event from a sponge. Impulse conduction in these sponges can be explained by the finding that hexactinellid tissues are syncytial. These results strongly suggest that hexactinellid sponges should be distinguished from other sponges at a high taxonomic level, and pose new questions for the evolution of intracellular transport mechanisms and excitability in the metazoa.

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Keywords

Hexactinellida, Sponges

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