Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges

Background: One of the hallmarks of multicellular organisms is the ability of their cells to trigger responses to the environment in a coordinated manner. In recent years primary cilia have been shown to be present as 'antennae' on almost all animal cells, and are involved in cell-to-cell signaling in development and tissue homeostasis; how this sophisticated sensory system arose has been little-studied and its evolution is key to understanding how sensation arose in the Animal Kingdom. Sponges (Porifera), one of the earliest evolving phyla, lack conventional muscles and nerves and yet sense and respond to changes in their fluid environment. Here we demonstrate the presence of non-motile cilia in sponges and studied their role as flow sensors. Results: Demosponges excrete wastes from their body with a stereotypic series of whole-body contractions using a structure called the osculum to regulate the water-flow through the body. In this study we show that short cilia line the inner epithelium of the sponge osculum. Ultrastructure of the cilia shows an absence of a central pair of microtubules and high speed imaging shows they are non-motile, suggesting they are not involved in generating flow. In other animals non-motile, 'primary', cilia are involved in sensation. Here we show that molecules known to block cationic ion channels in primary cilia and which inhibit sensory function in other organisms reduce or eliminate sponge contractions. Removal of the cilia using chloral hydrate, or removal of the whole osculum, also stops the contractions; in all instances the effect is reversible, suggesting that the cilia are involved in sensation. An analysis of sponge transcriptomes shows the presence of several transient receptor potential (TRP) channels including PKD channels known to be involved in sensing changes in flow in other animals. Together these data suggest that cilia in sponge oscula are involved in flow sensation and coordination of simple behaviour. Conclusions: This is the first evidence of arrays of non-motile cilia in sponge oscula. Our findings provide support for the hypothesis that the cilia are sensory, and if true, the osculum may be considered a sensory organ that is used to coordinate whole animal responses in sponges. Arrays of primary cilia like these could represent the first step in the evolution of sensory and coordination systems in metazoans. © 2014 Ludeman et al.; licensee BioMed Central Ltd

The mitochondrial genome of the hexactinellid sponge Aphrocallistes vastus: Evidence for programmed translational frameshifting

<p>Abstract</p> <p>Background</p> <p>Mitochondrial genomes (mtDNA) of numerous sponges have been sequenced as part of an ongoing effort to resolve the class-level phylogeny of the Porifera, as well as to place the various lower metazoan groups on the animal-kingdom tree. Most recently, the partial mtDNA of two glass sponges, class Hexactinellida, were reported. While previous phylogenetic estimations based on these data remain uncertain due to insufficient taxon sampling and accelerated rates of evolution, the mtDNA molecules themselves reveal interesting traits that may be unique to hexactinellids. Here we determined the first complete mitochondrial genome of a hexactinellid sponge, <it>Aphrocallistes vastus</it>, and compared it to published poriferan mtDNAs to further describe characteristics specific to hexactinellid and other sponge mitochondrial genomes.</p> <p>Results</p> <p>The <it>A. vastus </it>mtDNA consisted of a 17,427 base pair circular molecule containing thirteen protein-coding genes, divergent large and small subunit ribosomal RNAs, and a reduced set of 18 tRNAs. The <it>A. vastus </it>mtDNA showed a typical hexactinellid nucleotide composition and shared a large synteny with the other sequenced glass sponge mtDNAs. It also contained an unidentified open reading frame and large intergenic space region. Two frameshifts, in the <it>cox3 </it>and <it>nad6 </it>genes, were not corrected by RNA editing, but rather possessed identical shift sites marked by the extremely rare tryptophan codon (UGG) followed by the common glycine codon (GGA) in the +1 frame.</p> <p>Conclusion</p> <p>Hexactinellid mtDNAs have shown similar trends in gene content, nucleotide composition, and codon usage, and have retained a large gene syntenty. Analysis of the mtDNA of <it>A. vastus </it>has provided evidence diagnostic for +1 programmed translational frameshifting, a phenomenon disparately reported throughout the animal kingdom, but present in the hexactinellid mtDNAs that have been sequenced to date.</p

Effect of suspended sediments on the pumping rates of three species of glass sponge in situ

The largest known glass sponge reefs in Canada are within the Hecate Strait and Queen Charlotte Sound Glass Sponge Reefs Marine Protected Area (HSQCS-MPA) in British Columbia. However, human activities outside the core MPA boundaries, such as trawling, can create plumes of suspended sediments capable of travelling large distances. We studied the response of 3 glass sponge species to changes in suspended sediment concentrations (SSCs) at 170 m depth inside the HSQCS-MPA. Two species reduced excurrent flow rate in response to natural and experimentally induced increases in suspended sediment. Background suspended sediment levels were low and showed little variation (2.71 ± 0.09 mg l-1, mean ± SD). Species varied in the threshold of SSCs that triggered arrests. Sediment concentrations of 2.8-6.4 mg l-1 caused arrests in Rhabdocalyptus dawsoni, while Heterochone calyx did not arrest until concentrations reached 5-10 mg l-1. Very small, but prolonged increases of suspended sediments (<1 mg l-1 for R. dawsoni and 3.2 mg l-1 for H. calyx) caused arrests of several hours in R. dawsoni and prolonged periods of reduced flow in H. calyx. No arrests were observed in Farrea occa, even after repeated exposures up to 57 mg l-1. A sediment transport model showed that sediment concentrations can remain high enough to affect sponge behaviour as far as 2.39 km from the source of the plume. The results highlight the importance of understanding the biology of different species for establishment of adequate boundaries in MPAs.publishedVersio

Algal symbionts of the freshwater sponge Ephydatia muelleri

The freshwater sponge, Ephydatia muelleri, is an emerging model system for studying animal:microbe symbioses. Intracellular green microalgae are one of the more common symbionts that live in a facultative mutualism with E. muelleri. While these symbioses have long been known, the identity of the algal symbionts in E. muelleri cells has not been studied in detail. Here, we isolate and characterize endosymbiotic algae from E. muelleri collected from different geographic locations. We find that the algae can be transmitted through asexually produced gemmules and importantly that they can form symbioses with different, differentiated sponge cell types in the adult sponge. Our findings indicate that at least two algal lineages form endosymbioses with E. muelleri. One of the lineages includes species commonly found in samples from two locations in Canada and one in the United States (clade 1: closely related to Auxenochlorella pyrenoidosa). The other clade includes algae found in sponges from one site in Maine, USA, and Lewiniosphaera symbiontica, which is a strain isolated in 1956 from the freshwater sponge Spongilla. We compared microbiomes found in cultures of microalgae as well as the original sponge hosts, and found that very similar bacterial microbiomes associate with both clades (91 orders of Bacteria are shared among the samples we compared). The microbiomes found in the cultures resemble, with a high degree of overlap, the microbiome associated with the sponge host

Freshwater Sponges Have Functional, Sealing Epithelia with High Transepithelial Resistance and Negative Transepithelial Potential

Epithelial tissue — the sealed and polarized layer of cells that regulates transport of ions and solutes between the environment and the internal milieu — is a defining characteristic of the Eumetazoa. Sponges, the most ancient metazoan phylum [1], [2], are generally believed to lack true epithelia [3], [4], [5], but their ability to occlude passage of ions has never been tested. Here we show that freshwater sponges (Demospongiae, Haplosclerida) have functional epithelia with high transepithelial electrical resistance (TER), a transepithelial potential (TEP), and low permeability to small-molecule diffusion. Curiously, the Amphimedon queenslandica sponge genome lacks the classical occluding genes [5] considered necessary to regulate sealing and control of ion transport. The fact that freshwater sponge epithelia can seal suggests that either occluding molecules have been lost in some sponge lineages, or demosponges use novel molecular complexes for epithelial occlusion; if the latter, it raises the possibility that mechanisms for occlusion used by sponges may exist in other metazoa. Importantly, our results imply that functional epithelia evolved either several times, or once, in the ancestor of the Metazoa

The Physiology and Molecular Biology of Sponge Tissues

Sponges have become the focus of studies on molecular evolution and the evolution of animal body plans due to their ancient branching point in the metazoan lineage. Whereas our former understanding of sponge function was largely based on a morphological perspective, the recent availability of the first full genome of a sponge (Amphimedon queenslandica), and of the transcriptomes of other sponges, provides a new way of understanding sponges by their molecular components. This wealth of genetic information not only confirms some long-held ideas about sponge form and function but also poses new puzzles. For example, the Amphimedon sponge genome tells us that sponges possess a repertoire of genes involved in control of cell proliferation and in regulation of development. In vitro expression studies with genes involved in stem cell maintenance confirm that archaeocytes are the main stem cell population and are able to differentiate into many cell types in the sponge including pinacocytes and choanocytes. Therefore, the diverse roles of archaeocytes imply differential gene expression within a single cell ontogenetically, and gene expression is likely also different in different species; but what triggers cells to enter one pathway and not another and how each archaeocyte cell type can be identified based on this gene knowledge are new challenges. Whereas molecular data provide a powerful new tool for interpreting sponge form and function, because sponges are suspension feeders, their body plan and physiology are very much dependent on their physical environment, and in particular on flow. Therefore, in order to integrate new knowledge of molecular data into a better understanding the sponge body plan, it is important to use an organismal approach. In this chapter, we give an account of sponge body organization as it relates to the physiology of the sponge in light of new molecular data. We focus, in particular, on the structure of sponge tissues and review descriptive as well as experimental work on choanocyte morphology and function. Special attention is given to pinacocyte epithelia, cell junctions, and the molecules present in sponge epithelia. Studies describing the role of the pinacoderm in sensing, coordination, and secretion are reviewed. A wealth of recent work describes gene presence and expression patterns in sponge tissues during development, and we review this in the context of the previous descriptions of sponge morphology and physiology. A final section addresses recent findings of genes involved in the immune response. This review is far from exhaustive but intends rather to revisit for non-specialists key aspects of sponge morphology and physiology in light of new molecular data as a means to better understand and interpret sponge form and function today

Cytological basis of photoresponsive behavior in a sponge larva

Ontogenetic changes in the photoresponse of larvae from the demosponge Reneira sp. were studied by analyzing the swimming paths of individual larvae exposed to diffuse white light. Larvae swam upward upon release from the adult, but were negatively phototactic until at least 12 hours after release. The larval photoreceptors are presumed to be a posterior ring of columnar monociliated epithelial cells that possess 120-mum-long cilia and pigment-filled protrusions. A sudden increase in light intensity caused these cilia to become rigidly straight. If the light intensity remained high, the cilia gradually bent over the pigmented vesicles in the adjacent cytoplasm, and thus covered one entire pole of the larva. The response was reversed upon a sudden decrease in light intensity. The ciliated cells were sensitive to changes in light intensity in larvae of all ages. This response is similar to the shadow response in tunicate larvae or the shading of the photoreceptor in Euglena and is postulated to allow the larvae to steer away from brighter light to darker areas, such as under coral rubble-the preferred site of the adult sponge on the reef flat. In the absence of a coordinating system in cellular sponges, the spatial organization and autonomous behavior of the pigmented posterior cells control the rapid responses to light shown by these larvae

Cell counts and calculations

Microsoft Excel file containing 5 worksheets. Contains raw data (counts of new choanocytes labeled with EdU and counts of all choanocytes in a choanocyte chamber; counts of cells from the mesohyl), calculations of cell kinetics using the one-population steady state model (Nowakowski et al. 1989), and data and calculations used to create Figures 3, 4, and supporting tables 2, 3 and 4

Data from: The dorid nudibranchs Peltodoris lentiginosa and Archidoris odhneri as predators of glass sponges

The dorid nudibranchs Peltodoris lentiginosa and Archidoris odhneri were found on glass sponges (Porifera, Hexactinellida) during remotely operated vehicle surveys of three reefs in the Strait of Georgia, British Columbia, Canada. Eight nudibranchs were sampled from 2009 to 2011. Identification of sponge spicules found in their gut and fecal contents confirmed the nudibranchs to be predators of the reef-forming hexactinellids Aphrocallistes vastus and Heterochone calyx, as well as of the demosponge Desmacella austini, which encrusts skeletons of the glass sponges. Four of five nudibranchs dissected for gut content analysis had stomachs containing sponge spicules. Counts from high-definition video footage taken during systematic surveys done in 2009 showed that nudibranchs were found in only two of the three glass sponge reefs. These data provide the first quantitative evidence of a molluscan predator on glass sponges found outside of Antarctica, and establish the first trophic link between glass sponges and their associated community of animals in a sponge reef ecosystem on the western Canadian continental shelf

Data from: The dorid nudibranchs Peltodoris lentiginosa and Archidoris odhneri as predators of glass sponges

The dorid nudibranchs Peltodoris lentiginosa and Archidoris odhneri were found on glass sponges (Porifera, Hexactinellida) during remotely operated vehicle surveys of three reefs in the Strait of Georgia, British Columbia, Canada. Eight nudibranchs were sampled from 2009 to 2011. Identification of sponge spicules found in their gut and fecal contents confirmed the nudibranchs to be predators of the reef-forming hexactinellids Aphrocallistes vastus and Heterochone calyx, as well as of the demosponge Desmacella austini, which encrusts skeletons of the glass sponges. Four of five nudibranchs dissected for gut content analysis had stomachs containing sponge spicules. Counts from high-definition video footage taken during systematic surveys done in 2009 showed that nudibranchs were found in only two of the three glass sponge reefs. These data provide the first quantitative evidence of a molluscan predator on glass sponges found outside of Antarctica, and establish the first trophic link between glass sponges and their associated community of animals in a sponge reef ecosystem on the western Canadian continental shelf