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A new flow-regulating cell type in the Demosponge Tethya wilhelma - functional cellular anatomy of a leuconoid canal system.

Hammel JU, Nickel M - PLoS ONE (2014)

Bottom Line: We found a hitherto undescribed cell type, the reticuloapopylocyte, which is involved in flow regulation in the choanocyte chambers.These states permit a gradual regulation of the total apopylar opening area.Our study provides insights into the local and global flow conditions in the sponge canal system and thus enhances current understanding of related physiological processes.

View Article: PubMed Central - PubMed

Affiliation: Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Erbertstr. 1, 07743, Jena, Germany.

ABSTRACT
Demosponges possess a leucon-type canal system which is characterized by a highly complex network of canal segments and choanocyte chambers. As sponges are sessile filter feeders, their aquiferous system plays an essential role in various fundamental physiological processes. Due to the morphological and architectural complexity of the canal system and the strong interdependence between flow conditions and anatomy, our understanding of fluid dynamics throughout leuconoid systems is patchy. This paper provides comprehensive morphometric data on the general architecture of the canal system, flow measurements and detailed cellular anatomical information to help fill in the gaps. We focus on the functional cellular anatomy of the aquiferous system and discuss all relevant cell types in the context of hydrodynamic and evolutionary constraints. Our analysis is based on the canal system of the tropical demosponge Tethya wilhelma, which we studied using scanning electron microscopy. We found a hitherto undescribed cell type, the reticuloapopylocyte, which is involved in flow regulation in the choanocyte chambers. It has a highly fenestrated, grid-like morphology and covers the apopylar opening. The minute opening of the reticuloapopylocyte occurs in an opened, intermediate and closed state. These states permit a gradual regulation of the total apopylar opening area. In this paper the three states are included in a theoretical study into flow conditions which aims to draw a link between functional cellular anatomy, the hydrodynamic situation and the regular body contractions seen in T. wilhelma. This provides a basis for new hypotheses regarding the function of bypass elements and the role of hydrostatic pressure in body contractions. Our study provides insights into the local and global flow conditions in the sponge canal system and thus enhances current understanding of related physiological processes.

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Scanning electron micrograph of cellular structures in the choanocyte chamber.(A) Overview of a choanocyte chamber connected to an incurrent- and excurrent canal with the relevant cellular prosopylar and apopylar elements and the location of the new cell type: reticuloapopylocyte. (B) Circular arrangement of apopylar cells and the position adjacent to reticuloapopylocyte. Hydrodynamic sealing of apopylar velum and microvilli collar. (C) Arrangement of cilium bearing apopylar cells, choanocytes and reticuloapopylocytes in the choanocytic apopyle. (D) Detailed view of an apopylar cell with its cilium directing into the flow at the apopyle. (E) Detailed view of the apopylar velum and microvilli collar contact side which results in a hydrodynamic sealing. (F) Overview of prosopylar openings in the incurrent canal system. (G) Pore cell forming a prosopylar opening. In the background microvilli collars of choanocytes are visible.
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pone-0113153-g004: Scanning electron micrograph of cellular structures in the choanocyte chamber.(A) Overview of a choanocyte chamber connected to an incurrent- and excurrent canal with the relevant cellular prosopylar and apopylar elements and the location of the new cell type: reticuloapopylocyte. (B) Circular arrangement of apopylar cells and the position adjacent to reticuloapopylocyte. Hydrodynamic sealing of apopylar velum and microvilli collar. (C) Arrangement of cilium bearing apopylar cells, choanocytes and reticuloapopylocytes in the choanocytic apopyle. (D) Detailed view of an apopylar cell with its cilium directing into the flow at the apopyle. (E) Detailed view of the apopylar velum and microvilli collar contact side which results in a hydrodynamic sealing. (F) Overview of prosopylar openings in the incurrent canal system. (G) Pore cell forming a prosopylar opening. In the background microvilli collars of choanocytes are visible.

Mentions: Choanocyte chambers are almost globular in T. wilhelma and possess one apopylar and one to several prosopylar openings (Figure 4A). The number of choanocytes within a choanocyte chamber is dependent on chamber size and body size (∼50–90 choanocytes/chamber, 70±13 choanocytes/chamber (N = 15 taken from 4 specimens)). The choanocytic prosopyle is formed by an interstice between adjacent choanocytes which lack filopodial extensions, which means that the prosopyle itself lacks any kind of specialized choanocytic prosopylar structure (Figure 4A).


A new flow-regulating cell type in the Demosponge Tethya wilhelma - functional cellular anatomy of a leuconoid canal system.

Hammel JU, Nickel M - PLoS ONE (2014)

Scanning electron micrograph of cellular structures in the choanocyte chamber.(A) Overview of a choanocyte chamber connected to an incurrent- and excurrent canal with the relevant cellular prosopylar and apopylar elements and the location of the new cell type: reticuloapopylocyte. (B) Circular arrangement of apopylar cells and the position adjacent to reticuloapopylocyte. Hydrodynamic sealing of apopylar velum and microvilli collar. (C) Arrangement of cilium bearing apopylar cells, choanocytes and reticuloapopylocytes in the choanocytic apopyle. (D) Detailed view of an apopylar cell with its cilium directing into the flow at the apopyle. (E) Detailed view of the apopylar velum and microvilli collar contact side which results in a hydrodynamic sealing. (F) Overview of prosopylar openings in the incurrent canal system. (G) Pore cell forming a prosopylar opening. In the background microvilli collars of choanocytes are visible.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4237394&req=5

pone-0113153-g004: Scanning electron micrograph of cellular structures in the choanocyte chamber.(A) Overview of a choanocyte chamber connected to an incurrent- and excurrent canal with the relevant cellular prosopylar and apopylar elements and the location of the new cell type: reticuloapopylocyte. (B) Circular arrangement of apopylar cells and the position adjacent to reticuloapopylocyte. Hydrodynamic sealing of apopylar velum and microvilli collar. (C) Arrangement of cilium bearing apopylar cells, choanocytes and reticuloapopylocytes in the choanocytic apopyle. (D) Detailed view of an apopylar cell with its cilium directing into the flow at the apopyle. (E) Detailed view of the apopylar velum and microvilli collar contact side which results in a hydrodynamic sealing. (F) Overview of prosopylar openings in the incurrent canal system. (G) Pore cell forming a prosopylar opening. In the background microvilli collars of choanocytes are visible.
Mentions: Choanocyte chambers are almost globular in T. wilhelma and possess one apopylar and one to several prosopylar openings (Figure 4A). The number of choanocytes within a choanocyte chamber is dependent on chamber size and body size (∼50–90 choanocytes/chamber, 70±13 choanocytes/chamber (N = 15 taken from 4 specimens)). The choanocytic prosopyle is formed by an interstice between adjacent choanocytes which lack filopodial extensions, which means that the prosopyle itself lacks any kind of specialized choanocytic prosopylar structure (Figure 4A).

Bottom Line: We found a hitherto undescribed cell type, the reticuloapopylocyte, which is involved in flow regulation in the choanocyte chambers.These states permit a gradual regulation of the total apopylar opening area.Our study provides insights into the local and global flow conditions in the sponge canal system and thus enhances current understanding of related physiological processes.

View Article: PubMed Central - PubMed

Affiliation: Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Erbertstr. 1, 07743, Jena, Germany.

ABSTRACT
Demosponges possess a leucon-type canal system which is characterized by a highly complex network of canal segments and choanocyte chambers. As sponges are sessile filter feeders, their aquiferous system plays an essential role in various fundamental physiological processes. Due to the morphological and architectural complexity of the canal system and the strong interdependence between flow conditions and anatomy, our understanding of fluid dynamics throughout leuconoid systems is patchy. This paper provides comprehensive morphometric data on the general architecture of the canal system, flow measurements and detailed cellular anatomical information to help fill in the gaps. We focus on the functional cellular anatomy of the aquiferous system and discuss all relevant cell types in the context of hydrodynamic and evolutionary constraints. Our analysis is based on the canal system of the tropical demosponge Tethya wilhelma, which we studied using scanning electron microscopy. We found a hitherto undescribed cell type, the reticuloapopylocyte, which is involved in flow regulation in the choanocyte chambers. It has a highly fenestrated, grid-like morphology and covers the apopylar opening. The minute opening of the reticuloapopylocyte occurs in an opened, intermediate and closed state. These states permit a gradual regulation of the total apopylar opening area. In this paper the three states are included in a theoretical study into flow conditions which aims to draw a link between functional cellular anatomy, the hydrodynamic situation and the regular body contractions seen in T. wilhelma. This provides a basis for new hypotheses regarding the function of bypass elements and the role of hydrostatic pressure in body contractions. Our study provides insights into the local and global flow conditions in the sponge canal system and thus enhances current understanding of related physiological processes.

Show MeSH
Related in: MedlinePlus