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

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. / Graduate

Identiferoai:union.ndltd.org:uvic.ca/oai:dspace.library.uvic.ca:1828/8110
Date15 May 2017
CreatorsLeys, Sally Penelope
ContributorsMackie, George O.
Source SetsUniversity of Victoria
LanguageEnglish, English
Detected LanguageEnglish
TypeThesis
RightsAvailable to the World Wide Web

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