Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse ‘toolkit’ of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.
Sponges (Porifera) are among the earliest evolving metazoans. Their filter-feeding body plan based on choanocyte chambers organized into a complex aquiferous system is so unique among metazoans that it either reflects an early divergence from other animals prior to the evolution of features such as muscles and nerves, or that sponges lost these characters. Analyses of the Amphimedon and Oscarella genomes support this view of uniqueness-many key metazoan genes are absent in these sponges-but whether this is generally true of other sponges remains unknown. We studied the transcriptomes of eight sponge species in four classes (Hexactinellida, Demospongiae, Homoscleromorpha, and Calcarea) specifically seeking genes and pathways considered to be involved in animal complexity. For reference, we also sought these genes in transcriptomes and genomes of three unicellular opisthokonts, two sponges (A. queenslandica and O. carmela), and two bilaterian taxa. Our analyses showed that all sponge classes share an unexpectedly large complement of genes with other metazoans. Interestingly, hexactinellid, calcareous, and homoscleromorph sponges share more genes with bilaterians than with nonbilaterian metazoans. We were surprised to find representatives of most molecules involved in cell-cell communication, signaling, complex epithelia, immune recognition, and germ-lineage/sex, with only a few, but potentially key, absences. A noteworthy finding was that some important genes were absent from all demosponges (transcriptomes and the Amphimedon genome), which might reflect divergence from main-stem lineages including hexactinellids, calcareous sponges, and homoscleromorphs. Our results suggest that genetic complexity arose early in evolution as shown by the presence of these genes in most of the animal lineages, which suggests sponges either possess cryptic physiological and morphological complexity and/or have lost ancestral cell types or physiological processes.
This chapter reviews the major known monospecific and multispecific sponge aggregations in the world's oceans. They are shown to occur from the intertidal to abyssal depths, in tropical, temperate, and high latitudes and sometimes to create
Abstract. Early development and metamorphosis of Reniera sp., a haplosclerid demosponge, have been examined to determine how gastrulation occurs in this species, and whether there is an inversion of the primary germ layers at metamorphosis. Embryogenesis occurs by unequal cleavage of blastomeres to form a solid blastula consisting micro‐ and macromeres; multipolar migration of the micromeres to the surface of the embryo results in a bi‐layered embryo and is interpreted as gastrulation. Polarity of the embryo is determined by the movement of pigment‐containing micromeres to one pole of the embryo; this pole later becomes the posterior pole of the swimming larva. The bi‐layered larva has a fully differentiated monociliated outer cell layer, and a solid interior of various cell types surrounded by dense collagen. The pigmented cells at the posterior pole give rise to long cilia that are capable of responding to environmental stimuli. Larvae settle on their anterior pole. Fluorescent labeling of the monociliated outer cell layer with a cell‐lineage marker (CMFDA) demonstrates that the monociliated cells resorb their cilia, migrate inwards, and transdifferentiate into the choanocytes of the juvenile sponge, and into other amoeboid cells. The development of the flagellated choanocytes and other cells in the juvenile from the monociliated outer layer of this sponge's larva is interpreted as the dedifferentiation of fully differentiated larval cells—a process seen during the metamorphosis of other ciliated invertebrate larvae—not as inversion of the primary germ layers. These results suggest that the sequences of development in this haplosclerid demosponge are not very different than those observed in many cnidarians.
Glass sponges are conspicuous inhabitants of benthic communities in the cool waters of the Antarctic and north Pacific continental shelf. We used an ROV outfitted with a new device for simultaneous sampling of water inhaled and exhaled by the sponges to provide the first data on the nutritional ecology and metabolism of two glass sponge species in their natural deep-water habitat (120-160 m). Aphrocallistes vastus and Rhabdocalyptus dawsoni were found to be mostly bacteriovores, removing up to 95% of the bacteria (median removal was 79% for both species) and heterotrophic protists (,10 mm) from the water they filter. The relatively scarce microbial cells were efficiently selected from a 'soup' of suspended clay and detritus particles (microorganisms accounted for ,1% of the total ambient suspended solids). Removal of planktonic microorganisms (2.2 6 1.3 mmol carbon [C] C L 21 and 0.37 6 0.17 mmol nitrogen [N] L 21 ) accounted for the entire total organic C uptake and ammonium excretion by both species, with no evidence for dissolved organic uptake. Similar results were obtained in laboratory experiments in which dissolved organic C was directly measured. Despite the massive siliceous sponge skeleton, silica uptake was below detection levels (0.28 mmol L 21 ), supporting previous suggestions of low growth rates in Hexactinellida. Reported mean sponge abundances of .1 individual m 22 indicate that the sponge filtering activity may significantly affect the deep microbial community and benthic-pelagic mass exchange in some northeast Pacific fjords.Shallow-water benthic suspension feeders have an important role in the functioning of coastal and freshwater ecosystems (Gili and Coma 1998;Thorp and Casper 2003). The feeding activity of these animals can control the water column properties in shallow bays (Cloern 1982), rivers (Strayer et al. 1999), and fjords (Riisgå rd 1998), either directly (through grazing on the plankton community) or indirectly (by intensifying nutrient recycling or by selective removal of a specific planktonic component) (Thorp and Casper 2003). These activities are tightly coupled with hydrodynamic processes.Whereas the nutritional ecology of shallow suspension feeders has been well studied, equivalent studies of the nutritional ecology of deep-dwelling suspension feeders (below scuba depth) are scarce (Roberts and Hirshfield 2004) and rely largely on descriptive anatomy and in vitro experiments (e.g., Fiala-Medioni et al. 1986;Witte et al. 1997; Pile and Young 1999
Glass sponges are conspicuous members of the deep-sea fauna, but in the northeastern Pacific they form unusual reefs covering kilometers of seafloor. Individual sponges in fjords can process up to 10 m 3 water d 21 osculum 21 ; sponge reefs must therefore process considerable volumes and could significantly affect local water properties. We measured, in situ, the flux of carbon and nitrogen through Aphrocallistes vastus, the dominant reef-building species on Fraser Ridge reef, and calculated the energetics of feeding for all reefs in the Strait of Georgia, British Columbia. Sponges removed up to 90% of bacteria from the water and released ammonium. Because of the high density of sponges, high volumetric flow rates (up to 210 6 35 m 3 m 22 d 21 , mean 6 standard error, 95% confidence interval (CI) 132-288 m 3 m 22 d 21 ), and the efficient extraction of bacteria, we calculate a grazing rate of 165 6 29 m 3 m 22 d 21 (95% CI 102-228 m 3 m 22 d 21 ) for sponge reefs, the highest benthic grazing rate of any suspension-feeding community measured to date. Reefs of A. vastus extract seven times more carbon (3.4 6 1.4 g C m 22 d 21 ) than can be supported by vertical flux of total carbon alone and therefore require productive waters and steady currents to sustain their strong grazing. We calculate that modern sponge reefs in the northeastern Pacific remove 2.27 3 10 5 6 0.91 3 10 5 kg of bacterial carbon daily, nearly an order of magnitude less than the 1.38 3 10 6 6 0.55 3 10 6 kg removed by past sponge reefs estimated to have covered the continental shelf.
BackgroundOne 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.ResultsDemosponges 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.ConclusionsThis 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.
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