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Evolution of the innate and adaptive immune systems: relationships between potential immune molecules in the lowest metazoan phylum (Porifera) and those in vertebrates.

Porifera (sponge) form the lowest metazoan phylum and share a common ancestor with other metazoan phyla. In the present study, it is reported that sponges possess molecules that are similar in structure to those molecules involved in the immune system in mammals. Experiments with the marine sponges Geodia cydonium and Suberites domuncula have been performed on tissue (auto- and allografting) as well as on a cellular level. The studies revealed that sponges are provided with elements of the mammalian innate immune system, such as molecules containing scavenger receptor cysteine-rich domains. Furthermore, macrophage-derived cytokine-like molecules have been identified that are up-regulated during the grafting process. In addition, the (2'-5')oligoadenylate synthetase system exists in sponges. "Precursors" of the second type of immune response in mammals, the adaptive immune system, have been traced in sponges. It is shown that the expression of a lymphocyte-derived cytokine from mammals is up-regulated during non-self-recognition in S. domuncula. Finally, in G. cydonium, two classes of receptors that comprise Ig-like domains have been identified: the receptor tyrosine kinases and the non-enzymic sponge adhesion molecules. They contain two polymorphic Ig-like domains that are grouped to the variable set of immunoglobulins. The expression of these molecules is also up-regulated during the grafting process. It is concluded that sponges are already provided with a series of elements used in higher vertebrates for both the innate and the adaptive immune recognition.

2',5'-Oligoadenylate Synthetase↗

Cloning and sequencing of a Porifera partial cDNA coding for a short-chain collagen.

Collagen is present in Porifera, the lowest multicellular animals, but there is no information available on the primary structure of the collagen chains in this phylum. Developing fresh-water sponges have been used to extract total RNA in order to study in vitro translation products and to construct a cDNA library. Four translated proteins were collagenase-sensitive (200 kDa, 160 kDa, 81 kDa and 48 kDa). The cDNA library was screened with a human collagen probe and a clone, EmC4, covering 1.2 kb was isolated. Nucleotide sequencing of EmC4 revealed a conceptual open reading frame coding for 366 amino acids terminated by a stop codon TGA with 103 nucleotides downstream. The presumed translation product encoded contained several domains: a non-collagenous C-terminal domain of 156 amino acids with 9 cysteines, an uninterrupted collagenous domain of 171 amino acids, a non-collagenous domain of 16 amino acids with 3 cysteines and a probably incomplete N-terminal collagenous domain of 23 amino acids. Comparison with other sequences suggested that this collagen chain might belong to a non-fibrillar collagen family which evolved into several sub-families giving rise to nematode cuticular collagens, and type IV collagens.

Amino Acid Sequence↗

Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria.

BACKGROUND: The mitochondrial genome of Metazoa is usually a compact molecule without introns. Exceptions to this rule have been reported only in corals and sea anemones (Cnidaria), in which group I introns have been discovered in the cox1 and nad5 genes. Here we show several lines of evidence demonstrating that introns can also be found in the mitochondria of sponges (Porifera). RESULTS: A 2,349 bp fragment of the mitochondrial cox1 gene was sequenced from the sponge Tetilla sp. (Spirophorida). This fragment suggests the presence of a 1143 bp intron. Similar to all the cnidarian mitochondrial introns, the putative intron has group I intron characteristics. The intron is present in the cox1 gene and encodes a putative homing endonuclease. In order to establish the distribution of this intron in sponges, the cox1 gene was sequenced from several representatives of the demosponge diversity. The intron was found only in the sponge order Spirophorida. A phylogenetic analysis of the COI protein sequence and of the intron open reading frame suggests that the intron may have been transmitted horizontally from a fungus donor. CONCLUSION: Little is known about sponge-associated fungi, although in the last few years the latter have been frequently isolated from sponges. We suggest that the horizontal gene transfer of a mitochondrial intron was facilitated by a symbiotic relationship between fungus and sponge. Ecological relationships are known to have implications at the genomic level. Here, an ecological relationship between sponge and fungus is suggested based on the genomic analysis.

Animals↗

Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera).

BACKGROUND: Sponges (Porifera) are nerve- and muscleless metazoa, but display coordinated motor reactions. Therefore, they represent a valuable phylum to investigate coordination systems, which evolved in a hypothetical Urmetazoon prior to the central nervous system (CNS) of later metazoa. We have chosen the contractile and locomotive species Tethya wilhelma (Demospongiae, Hadromerida) as a model system for our research, using quantitative analysis based on digital time lapse imaging. In order to evaluate candidate coordination pathways, we extracorporeally tested a number of chemical messengers, agonists and antagonists known from chemical signalling pathways in animals with CNS. RESULTS: Sponge body contraction of T. wilhelma was induced by caffeine, glycine, serotonine, nitric oxide (NO) and extracellular cyclic adenosine monophosphate (cAMP). The induction by glycine and cAMP followed patterns varying from other substances. Induction by cAMP was delayed, while glycine lead to a bi-phasic contraction response. The frequency of the endogenous contraction rhythm of T. wilhelma was significantly decreased by adrenaline and NO, with the same tendency for cAMP and acetylcholine. In contrast, caffeine and glycine increased the contraction frequency. The endogenous rhythm appeared irregular during application of caffeine, adrenaline, NO and cAMP. Caffeine, glycine and NO attenuated the contraction amplitude. All effects on the endogenous rhythm were neutralised by the washout of the substances from the experimental reactor system. CONCLUSION: Our study demonstrates that a number of chemical messengers, agonists and antagonists induce contraction and/or modulate the endogenous contraction rhythm and amplitude of our nerveless model metazoon T. wilhelma. We conclude that a relatively complex system of chemical messengers regulates the contraction behaviour through auto- and paracrine signalling, which is presented in a hypothetical model. We assume that adrenergic, adenosynergic and glycinergic pathways, as well as pathways based on NO and extracellular cAMP are candidates for the regulation and timing of the endogenous contraction rhythm within pacemaker cells, while GABA, glutamate and serotonine are candidates for the direct coordination of the contractile cells.

Journal Article↗

Cytological examination of reduction bodies of Corvomeyenia carolinensis Harrison (porifera: spongillidae).

Freshwater sponges, Corvomeyenia carolinensis Harrison, were placed into tap water to induce degenerative reduction body formation. Reduction bodies were examined using light and electron microscopy in order to define their histochemical and ultrastructural characteristics. The reduction body of freshwater sponges is an extremely simple developmental system consisting primarily of an archeocyte reserve delimited by a simple squamous pinacoderm. The freshwater sponge reduction body displays many similarities to overwintering phases of marine sponges. The system presents an unusually straightforward vehicle for investigations of degeneration and regeneration as processes in developmental biology and may represent a reasonable vehicle in which to examine the process of the genesis of lysosomes.

Animals↗

Ultrastructural study of the mature egg of the marine sponge Stelletta grubii (Porifera Demospongiae).

Stelletta grubii is an oviparous demosponge, which, during its reproductive period from summer to autumn, has small eggs (80-90 microns) dispersed uniformly in the mesohyl. The nucleolated nucleus is surrounded by dictyosomes containing small vesicles, which contribute to form reserve material. Vesicles, numerous food vacuoles, and groups of mitochondria are observed in the granular cytoplasm. Electron-dense yolk inclusions and lipids are found peripherally. The cortical portion of the egg cytoplasm possesses vacuoles with fibrillar contents. The egg forms pseudopodia, which could permit the capture of numerous bacteria present in the surrounding mesohyl. A thick layer of collagen fibrils, including lophocytes, separates the egg from the surrounding sponge mesohyl. Ultrastructural analysis has demonstrated the presence both of cellular components capable of autosynthetic activity (nutrient vesicles) and of phagocytosis mechanisms (pseudopod capture of bacteria) for the storage of nutrients by the egg.

Animals↗

Ultrastructural study of the mature egg of Tethya citrina Sarà and Melone (Porifera, Demospongiae).

Tethya citrina is an oviparous demosponge in which eggs are distributed in clumps within the choanosome. The cytoplasm of the mature egg presents a peripheral cortex consisting of a slightly granular layer sandwiched between two densely granular, vesiculated ones. The cortex probably has a specialized, trophic function. Mesohyl bacteria are phagocyted at the egg surface, included in vacuoles, and transferred across the cortical sheath toward the inner cytoplasm. The region of the egg extending between the cortex and the nucleus shows a lacunary system mostly developed beneath the cortical envelope. The noncortical cytoplasm also contains lipid droplets, dense rodlike bodies, and phagosomelike granules. Most of the latter are probably autophagosomes, forming lacunae and supporting autosynthetic vitellogenesis. Rodlike inclusions are probably proteinaceous; they likely originate within the phagosomes and represent the actual yolk material.

Animals↗

Molecular cloning of silicatein gene from marine sponge Petrosia ficiformis (Porifera, Demospongiae) and development of primmorphs as a model for biosilicification studies.

In some sponges peculiar proteins called silicateins catalyze silica polymerization in ordered structures, and their study is of high interest for possible biotechnological applications in the nanostructure industry. In this work we describe the isolation and the molecular characterization of silicatein from spicules of Petrosia ficiformis, a common Mediterranean sponge, and the development of a cellular model (primmorphs) suitable for in vitro studies of silicatein gene regulation. The spicule of P. ficiformis contains an axial filament composed of 2 insoluble proteins, of 30 and 23 kDa. The 23-kDa protein was characterized, and the full-length cDNA was cloned. The putative amino acid sequence has high homology with previously described silicateins from other sponge species and also is very similar to cathepsins, a cystein protease family. Finally, P. ficiformis primmorphs express the silicatein gene, suggesting that they should be a good model for biosilicification studies.

Amino Acid Sequence↗