Natural hybrid silica/protein superstructure at atomic resolution.

Formation of highly symmetric skeletal elements in demosponges, called spicules, follows a unique biomineralization mechanism in which polycondensation of an inherently disordered amorphous silica is guided by a highly ordered proteinaceous scaffold, the axial filament. The enzymatically active proteins, silicateins, are assembled into a slender hybrid silica/protein crystalline superstructure that directs the morphogenesis of the spicules. Furthermore, silicateins are known to catalyze the formation of a large variety of other technologically relevant organic and inorganic materials. However, despite the biological and biotechnological importance of this macromolecule, its tertiary structure was never determined. Here we report the atomic structure of silicatein and the entire mineral/organic hybrid assembly with a resolution of 2.4 Å. In this work, the serial X-ray crystallography method was successfully adopted to probe the 2-µm-thick filaments in situ, being embedded inside the skeletal elements. In combination with imaging and chemical analysis using high-resolution transmission electron microscopy, we provide detailed information on the enzymatic activity of silicatein, its crystallization, and the emergence of a functional three-dimensional silica/protein superstructure in vivo. Ultimately, we describe a naturally occurring mineral/protein crystalline assembly at atomic resolution.

Molecular complexity and gene expression controlling cell turnover during a digestive cycle of carnivorous sponge Lycopodina hypogea.

Lycopodina hypogea is a carnivorous sponge that tolerates laboratory husbandry very well. During a digestion cycle, performed without any digestive cavity, this species undergoes spectacular morphological changes leading to a total regression of long filaments that ensure the capture of prey and their reformation at the end of the cycle. This phenomenon is a unique opportunity to analyze the molecular and cellular determinants that ensure digestion in the sister group of all other metazoans. Using differential transcriptomic analysis coupled with cell biology studies of proliferation, differentiation, and programmed cell deaths (i.e., autophagy and the destructive/constructive function of apoptosis), we demonstrate that the molecular and cellular actors that ensure digestive homeostasis in a sister group of all remaining animals are similar in variety and complexity to those controlling tissue homeostasis in higher vertebrates. During a digestion cycle, most of these actors are finely tuned in a coordinated manner. Our data benefits from complementary approaches coupling in silico and cell biology studies and demonstrate that the nutritive function is provided by the coordination of molecular network that impacts the cells turnover in the entire organism.

Sponge digestive system diversity and evolution: filter feeding to carnivory.

Sponges are an ancient basal life form, so understanding their evolution is key to understanding all metazoan evolution. Sponges have very unusual feeding mechanisms, with an intricate network of progressively optimized filtration units: from the simple choanocyte lining of a central cavity, or spongocoel, to more complex chambers and canals. Furthermore, in a single evolutionary event, a group of sponges transitioned to carnivory. This major evolutionary transition involved replacing the filter-feeding apparatus with mobile phagocytic cells that migrate collectively towards the trapped prey. Here, we focus on the diversity and evolution of sponge nutrition systems and the amazing adaptation to carnivory.

Bromotryptamine and Bromotyramine Derivatives from the Tropical Southwestern Pacific Sponge Narrabeena nigra.

So far, the Futuna Islands located in the Central Indo-Pacific Ocean have not been inventoried for their diversity in marine sponges and associated chemical diversity. As part of the Tara Pacific expedition, the first chemical investigation of the sponge Narrabeena nigra collected around the Futuna Islands yielded 18 brominated alkaloids: seven new bromotryptamine derivatives 1-7 and one new bromotyramine derivative 8 together with 10 known metabolites of both families 9-18. Their structures were deduced from extensive analyses of nuclear magnetic resonance (NMR) and high-resolution mass spectrometry (HRMS) data. In silico metabolite anticipation using the online tool MetWork revealed the presence of a key and minor biosynthetic intermediates. These 18 compounds showed almost no cytotoxic effect up to 10 µM on human neuroblastoma SH-SY5Y and microglia BV2 cells, and some of them exhibited an interesting neuroprotective activity by reducing oxidative damage.

The systematics of carnivorous sponges.

Carnivorous sponges are characterized by their unique method of capturing mesoplanktonic prey coupled with the complete or partial reduction of the aquiferous system characteristic of the phylum Porifera. Current systematics place the vast majority of carnivorous sponges within Cladorhizidae, with certain species assigned to Guitarridae and Esperiopsidae. Morphological characters have not been able to show whether this classification is evolutionary accurate, and whether carnivory has evolved once or in several lineages. In the present paper we present the first comprehensive molecular phylogeny of the carnivorous sponges, interpret these results in conjunction with morphological characters, and propose a revised classification of the group. Molecular phylogenies were inferred using 18S rDNA and a combined dataset of partial 28S rDNA, COI and ALG11 sequences. The results recovered carnivorous sponges as a clade closely related to the families Mycalidae and Guitarridae, showing family Cladorhizidae to be monophyletic and also including carnivorous species currently placed in other families. The genus Lycopodina is resurrected for species currently placed in the paraphyletic subgenus Asbestopluma (Asbestopluma) featuring forceps spicules and lacking sigmas or sigmancistras. The genera Chondrocladia and Cladorhiza are found to be monophyletic. However, results indicate that the subgenus Chondrocladia is polyphyletic with respect to the subgenera Meliiderma and Symmetrocladia. Euchelipluma, formerly Guitarridae, is retained, but transferred to Cladorhizidae. The four known carnivorous species currently in Esperiopsis are transferred to Abyssocladia. Neocladia is a junior homonym and is here renamed Koltunicladia. Our results provide strong evidence in support of the hypothesis that carnivory in sponges has evolved only once. While spicule characters mostly reflect monophyletic groups at the generic level, differences between genera represent evolution within family Cladorhizidae rather than evolution of carnivory in separate lineages. Conflicting spicule characters can be reinterpreted to support the inclusion of all carnivorous sponges within Cladorhizidae, and a carnivorous habit should thus be considered the main diagnostic character in systematic classification.

Netamines O-S, Five New Tricyclic Guanidine Alkaloids from the Madagascar Sponge Biemna laboutei, and Their Antimalarial Activities.

In our continuing program to isolate new compounds from the Madagascar sponge Biemna laboutei, five new tricyclic guanidine alkaloids, netamines O - S (1-5, resp.), have been identified together with the known compounds netamine E (6) and mirabilin J (7). The structures of all new netamines were assigned on the basis of spectroscopic analyses. Their relative configurations were established by analysis of ROESY data and comparison with literature data. Netamines O, P, and Q, which were isolated in sufficient quantities, were tested for their cytotoxic activities against KB cells and their activities against the malaria parasite Plasmodium falciparum. Netamines O and Q were found to be moderately cytotoxic. Netamines O, P, and Q exhibited antiplasmodial activities with IC50 values of 16.99 ± 4.12, 32.62 ± 3.44, and 8.37 ± 1.35 µM, respectively.

Netamines H-N, tricyclic alkaloids from the marine sponge Biemna laboutei and their antimalarial activity.

Chemical examination of the CH2Cl2-MeOH (1:1) extract of the Madagascar sponge Biemna laboutei resulted in the isolation of seven new tricyclic alkaloids, netamines H-N (1-7), along with the known netamine G and mirabilins A, C, and F. Their structures were elucidated by interpretation of 1D and 2D NMR spectra and HRESIMS data. All compounds were evaluated for their cytotoxicity against KB cells and their antiplasmodial activity. Netamine M (6) was found to be cytotoxic, with an IC50 value in the micromolar range, and netamine K (4) exhibited activity against Plasmodium falciparum with an IC50 value of 2.4 µM.

A new species of Abyssocladia (Porifera, Demospongiae, Poecilosclerida, Cladorhizidae) and other carnivorous sponges from the far eastern Solomon Islands.

Two species, one each of Abyssocladia Lévi, 1964, and Asbestopluma Topsent, 1901, are recorded from the far eastern Solomon Islands for the first time. Abyssocladia lakwollii sp. nov. is characterized by the pedunculate disc-shape of the body, the unusually large size of the isochelae I microscleres, and by the shape of the cleistochelae with crossed central teeth. Asbestopluma (A.) desmophora Kelly & Vacelet, 2011, first described from a seamount on Macquarie Ridge (Australia EEZ) and eastern waters to the north and south of New Zealand, is also recorded from the far eastern Solomon Islands. The specimens differ only slightly from their southern counterparts in dimensions of some spicules, and in the ornamentation detail of the basal teeth of the large and small anisochelae. 

Deep metazoan phylogeny: when different genes tell different stories.

Molecular phylogenetic analyses have produced a plethora of controversial hypotheses regarding the patterns of diversification of non-bilaterian animals. To unravel the causes for the patterns of extreme inconsistencies at the base of the metazoan tree of life, we constructed a novel supermatrix containing 122 genes, enriched with non-bilaterian taxa. Comparative analyses of this supermatrix and its two non-overlapping multi-gene partitions (including ribosomal and non-ribosomal genes) revealed conflicting phylogenetic signals. We show that the levels of saturation and long branch attraction artifacts in the two partitions correlate with gene sampling. The ribosomal gene partition exhibits significantly lower saturation levels than the non-ribosomal one. Additional systematic errors derive from significant variations in amino acid substitution patterns among the metazoan lineages that violate the stationarity assumption of evolutionary models frequently used to reconstruct phylogenies. By modifying gene sampling and the taxonomic composition of the outgroup, we were able to construct three different yet well-supported phylogenies. These results show that the accuracy of phylogenetic inference may be substantially improved by selecting genes that evolve slowly across the Metazoa and applying more realistic substitution models. Additional sequence-independent genomic markers are also necessary to assess the validity of the phylogenetic hypotheses.

Nepheliosyne B, a new polyacetylenic acid from the new caledonian marine sponge Niphates sp.

A new C47 polyoxygenated acetylenic acid, nepheliosyne B (2), along with the previously described nepheliosyne A (1), have been isolated from the New Caledonian marine sponge Niphates sp. Their structures have been elucidated on the basis of extensive spectroscopic analyses. These metabolites exhibited a moderate cytotoxicity against K562, U266, SKM1, and Kasumi cancer cell lines.

A giant foraminifer that converges to the feeding strategy of carnivorous sponges: Spiculosiphon oceana sp. nov. (Foraminifera, Astrorhizida).

The foraminifer Spiculosiphon oceana sp. nov. is a giant (>4 cm) agglutinated astrorhizid, which makes the second known species of this unusual genus and its first Mediterranean record. It has a peculiar stalked, capitate, monothalamous test. Bleach digestion and X-ray microanalysis indicated the test to be made exclusively of siliceous sponge spicules agglutinated in organic cement. The organism stands on a hollow, 4 cm long, 0.5 cm thick stalk built with highly selected, long and thin spicule fragments, tightly cemented together in parallel to the main axis of the stalk. The proximal end of the stalk is closed and slightly expanded into a bulb-like structure, designed to penetrate between the sand grains and maintaining the test upright while avoiding a permanent attachment to the substratum. The distal stalk end becomes a hollow, globe-like structure that contains the main protoplasm. The globelike region is built with loosely agglutinated and irregularly-shaped spicules, allowing extrusion of the pseudopodia through the cavities between the spicules. The globelike structure also serves as an anchoring basis, from which long and thin, solid tracts protrude radially to make a spherical crown that attains about 4 mm in total diameter. The radiating tracts are built with highly selected aciculate spicule fragments held together with a translucent organic cement. They provide skeletal support for the extension of a crown of pseudopodia into the water column. This arrangement is thought to enhance the chances of the pseudopodia to contact demersal planktonic prey. In summary, Spiculosiphon species collect and arrange sponge spicules with high selectivity to recreate a body morphology that strongly converges to that of some carnivorous sponges, which allows these predatory foraminifera to exploit a prey capturing strategy similar to that of the carnivorous sponges. This idea is also consistent with our report of an additional, yet undetermined, Spiculosiphon species occurring in the same sublittoral Mediterranean cave where carnivorous sponges were first discovered.

New species of Abyssocladia and two new cladorhizid genera (Porifera, Cladorhizidae) from New Zealand and Australia.

Seamounts on subantarctic New Zealand's Macquarie Ridge, including parts of Australia's Exclusive Economic Zone surrounding Macquarie Island, have been demonstrated to be a rich source of new species of carnivorous sponges (Demospongiae Sollas, Poecilosclerida Topsent, Cladorhizidae Dendy). Four new species of Abyssocladia Lévi, 1964, are described from Macquarie Ridge seamounts and at other disparate locations: Abyssocladia lanceola sp. nov. from Seamounts 7, 8, and 9 (Australia EEZ), Seamount 10 (International Waters), and the South Tasman Rise; Abyssocladia rowdeni sp. nov., first collected from diffuse hydrothermal vent sites at Brothers Seamount on the Southern Kermadec Ridge and recorded here from the non-venting seamounts on Chatham Rise to the east of the South Island of New Zealand; Abyssocladia tumulorum sp. nov., found exclusively on the Chatham Rise; and Abyssocladia sonnae sp. nov. from Monowai Seamount on the Tonga-Kermadec Ridge in International Waters, also found, surprisingly, on Macquarie Ridge's Seamount 8 (Australia EEZ). Patriciacladia gen. nov. has been established for a new species of Cladorhizidae discovered on Macquarie Ridge and Chatham Rise. Patriciacladia enigmatica gen. et sp. nov. is highly unusual in that it possesses palmate isochelae not typically found in Cladorhizidae and has a long branch in phylogenetic analysis of the family, supporting the establishment of a new genus and species for Abyssocladia n. sp. B (QM G339872, was NIWA 41033): 28S rDNA: LN870583, COI: LN870445, Macquarie Ridge) in Hestetun et al. (2016a: table 1; 2017: fig. 15). The discovery of two new species, again from the Macquarie Ridge and other New Zealand locations, expands support for the establishment of a new genus, Australocladia gen. nov., which contains several additional species nested as a monophyletic clade within the large, heterogenous, and paraphyletic Abyssocladia clade in molecular phylogenetic analyses. Australocladia sphaerichela gen. et sp. nov. and Au. alopecura gen. et sp. nov. both possess spherical abyssochelae, funnel-shaped expansions which may contain spermatophores on the body, substrongyles in the attachment base, and a generally southern hemisphere distribution.

New lithistid sponge of the genus Sollasipelta (Porifera, Demospongiae,Tetractinellida, Neopeltidae) from submarine caves of the Ryukyu Islands,southwestern Japan, with redescription of S. sollasi.

A new species of 'lithistid' (rock sponge) Sollasipelta subterranea sp. nov. is described from near-shore submarine caves of Okinawa and Shimoji Islands, the Ryukyu Islands, southwestern Japan. This new species is characterized by the smooth dentate ectosomal pseudophyllotriaenes, slender choanosomal oxea/style/subtylostyles and two types of amphiasters, one of which is in two size classes. Sollasipelta subterranea sp. nov. is morphologically closest to Sollasipelta sollasi (Lévi & Lévi, 1989), known from the Philippines deep sea, and our examination of the type specimen of S. sollasi revealed that the pseudophyllotriaenes and desmas are substantially different between the two species, and both species possess two types of amphiasters, one of which has two size classes. Sollasipelta cavernicola (Vacelet & Vasseur, 1965) and S. punctata (Lévi & Lévi, 1983) are transferred to the genus Daedalopelta Sollas, 1888, based on possession of one type of amphiastes as microscleres. Sollasipelta mixta (Vacelet, Vasseur and Lévi, 1976) is formally transferred to the genus Neopelta Schmidt, 1880, based on the morphological characters. A key to species of the genus Sollasipelta Van Soest & Hooper, 2020 is also provided. Sollasipelta subterranea sp. nov. represents the first 'lithistid' sponge from submarine caves of the Western Pacific and the first species of sponge inhabiting anchialine cave environments in the Indo-West Pacific. This is also a new record of the family Neopeltidae from Japanese waters.

The Station Marine d'Endoume, Marseille: 150 years of natural history.

When marine natural sciences began to be the concern of most European scientists, in the middle of the 19th century, Marseille, in southern France, was no exception. The creation, ca. 150 years ago, of the first Zoology Laboratory of the Faculty of Sciences of Marseille took place in 1868. Under the leadership of Antoine-Fortuné Marion, it soon led to the creation of the Station Marine d'Endoume (SME) in 1889. Marion's pioneering work survived both world wars and was then taken to another dimension by Jean-Marie Pérès, head of the marine station from 1948 to 1983. This institution is still alive to date. We here inventoried all the taxa described by SME scientists (1870 to 2021) and arranged them in a public database. Three main periods of activity at the SME are described, as well as the focus made through time to different groups of taxa, selected ecosystems, or biogeographic areas. Through many examples, it was possible to document how these naturalistic, taxonomic descriptions contributed to a broader scientific knowledge within this period. Finally, we discussed trends in taxonomic and naturalistic research, based on the SME experience.

Cell death and renewal during prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Poecilosclerida).

The sponge Asbestopluma hypogea is unusual among sponges due to its peculiar carnivorous feeding habit. During various stages of its nutrition cycle, the sponge is subjected to spectacular morphological modifications. Starved animals are characterized by many elongated filaments, which are crucial for the capture of prey. After capture, and during the digestion process, these filaments actively regress before being regenerated during a subsequent period of starvation. Here, we demonstrate that these morphological events rely on a highly dynamic cellular turnover, implying a coordinated sequence of programmed cell death (apoptosis and autophagy), cell proliferation and cell migration. A candidate niche for cell renewal by stem cell proliferation and differentiation was identified at the base of the sponge peduncle, characterized by higher levels of BrdU/EdU incorporation. Therefore, BrdU/EdU-positive cells of the peduncle base are candidate motile cells responsible for the regeneration of the prey-capturing main sponge body, i.e. the dynamic filaments. Altogether, our results demonstrate that dynamics of cell renewal in sponge appear to be regulated by cellular mechanisms as multiple and complex as those already identified in bilaterian metazoans.

The Homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology: model sponge Oscarella lobularis.

Sponges branch basally in the metazoan phylogenetic tree and are believed to be composed of four distinct lineages with still uncertain relationships. Indeed, some molecular studies propose that Homoscleromorpha may be a fourth Sponge lineage, distinct from Demospongiae in which they were traditionally classified. They harbour many features that distinguish them from other sponges and are more evocative of those of the eumetazoans. They are notably the only sponges to possess a basement membrane with collagen IV and specialized cell-junctions, thus possessing true epithelia. Among Homoscleromorphs, we have chosen Oscarella lobularis as a model species. This common and easily accessible sponge is characterized by relatively simple histology and cell composition, absence of skeleton, and strongly pronounced epithelial structure. In this review, we explore the specific features that make O. lobularis a promising homoscleromorph sponge model for evolutionary and developmental researches.

A new hydroxylated nonaprenylhydroquinone from the Mediterranean marine sponge Sarcotragus spinosulus.

Chemical investigation of the Mediterranean sponge Sarcotragus spinosulus led to the isolation of a new hydroxylated nonaprenylhydroquinone, along with two known metabolites, hepta- and octaprenylhydroquinones. The structure of the new metabolite was assigned by extensive 1D and 2D NMR analyses and MS studies. The antileukemic effect of the three compounds towards the chronic myelogenous leukemia (CML) cells line K562 was also evaluated.

Structure elucidation of the new citharoxazole from the Mediterranean deep-sea sponge Latrunculia (Biannulata) citharistae.

Citharoxazole (1), a new batzelline derivative featuring a benzoxazole moiety, was isolated from the Mediterranean deep-sea sponge Latrunculia (Biannulata) citharistae Vacelet, 1969, together with the known batzelline C (2). This is the first chemical study of a Mediterranean Latrunculia species and the benzoxazole moiety is unprecedented for this family of marine natural products. The structure was mainly elucidated by the interpretation of NMR spectra and especially HMBC correlations.

First record of the genus Discorhabdella (Porifera, Demospongiae, Poecilosclerida, Crambeidae) from Sagami Bay, Japan with description of two new species.

Two new species of Discorhabdella are described from Sagami Bay, Japan. Discorhabdella has been suggested to have an ancient Tethyan origin according to discovery of their unique pseudoastrose acanthostyles from late Eocene to Oligocene deposits. This is the first record of the genus from the northwest Pacific and first record of the family Crambeidae from Japan. Discorhabdellahispida sp. nov. is distinctive within the genus by possession of special sigmoid microscleres and C-shaped isochelae with short alae. Discorhabdellamisakiensis sp. nov. is characterized by short choanosomal subtylostyles, and their length overlapped with that of the ectosomal subtylostyles. Only one other species, Discorhabdellatuberosocapitata (Topsent, 1890), has the same spicule composition. However, all spicule types are larger in D.tuberosocapitata than those of D.misakiensis sp. nov., and the shape of the isochelae is different: the alae are more widely opened in D.tuberosocapitata. An identification key to species of the genus Discorhabdella is also provided. The discovery of two new species from warm temperate northwest Pacific extends the geographical distribution of the genus Discorhabdella.

New carnivorous sponges of the genus Abyssocladia (Demospongiae, Poecilosclerida, Cladorhizidae) from Myojin Knoll, Izu-Ogasawara Arc, southern Japan.

Two new species of carnivorous sponges of the genus Abyssocladia are described. These sponges were collected from Myojin Knoll, Izu-Ogasawara (Izu-Bonin) Arc, in southern Japan. Detailed morphological observation based on specimen both in situ and preserved revealed functional differentiation of spicule distribution. Abyssocladia natsushimae sp. nov. is distinct within the genus in its mop-like gross morphology, large body size, and soft tissue packed with numerous microspined microstrongyles. Abyssocladia myojinensis sp. nov. is characterized by possession of both typical abyssochelae and palmate abyssochelae. This is the first record of the genus from Japan.