Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization

Enzymes of the α-carbonic anhydrase gene family (CAs) are essential for the deposition of calcium carbonate biominerals. In calcareous sponges (phylum Porifera, class Calcarea), specific CAs are involved in the formation of calcite spicules, a unique trait and synapomorphy of this class. However, detailed studies on the CA repertoire of calcareous sponges exist for only two species of one of the two Calcarea subclasses, the Calcaronea. The CA repertoire of the second subclass, the Calcinea, has not been investigated so far, leaving a considerable gap in our knowledge about this gene family in Calcarea. Here, using transcriptomic analysis, phylogenetics, and in situ hybridization, we study the CA repertoire of four additional species of calcareous sponges, including three from the previously unsampled subclass Calcinea. Our data indicate that the last common ancestor of Calcarea had four ancestral CAs with defined subcellular localizations and functions (mitochondrial/cytosolic, membrane-bound, and secreted non-catalytic). The evolution of membrane-bound and secreted CAs involved gene duplications and losses, whereas mitochondrial/cytosolic and non-catalytic CAs are evidently orthologous genes. Mitochondrial/cytosolic CAs are biomineralization-specific genes recruited for biomineralization in the last common ancestor of calcareous sponges. The spatial–temporal expression of these CAs differs between species, which may reflect differences between subclasses or be related to the secondary thickening of spicules during biomineralization that does not occur in all species. With this study, we extend the understanding of the role and the evolution of a key biomineralization gene in calcareous sponges.

Microfacies and biostratigraphy of an Upper Triassic Dachstein limestone fore-reef block in the Jurassic Sirogojno carbonate-clastic Mélange (Zlatibor Mt., SW Serbia)

In the late Middle to early Late Jurassic carbonate-clastic Sirogojno M?lange in the Zlatibor Mountain there is one roughly 35 m thick overturned block with an intact Late Triassic fore-reefal Dachstein Limestone succession that was studied here for its biostratigraphic age, faunal content and microfacies characteristics. The succession starts with coarse-grained rudstones followed by meter-sized reefal blocks intercalated in partly layered resedimented grainstones and packstones with abundant reef-building organisms like calcareous sponges, corals and encrusting organisms. Inside this part of the succession open-marine influenced layers are rare. The succession continues with a partly turbiditic sequence and chaotic rudstones, densely packed with reef-derived material like broken reef-building organisms and shallow-water material like gastropods, bivalves and foraminifers. Grainstones with clear open-marine influence (e.g., thin-shelled bivalves, crinoids, conodonts) appear in between those rudstones, in cases lumachelle layers consisting of halobiids were deposited. To the end of the succession some layers show turbiditic bedding with mixed shallow- water and deep-marine grains and organisms, i.e. filaments and crinoids. On base of conodonts, foraminifers, calcareous algae, holothurians and halobiids throughout the whole studied succession, a Middle Norian (Alaunian) to Rhaetian 1, most probably a Late Norian (Sevatian) age can be assigned to this forereefal Dachstein Limestone succession, with a similar sedimentation pattern like Late Triassic Dachstein fore-reef limestone facies, e.g., in the Northern Calcareous Alps or the eastern Southern Alps. The study of this block in the Sirogojno M?lange closes an important gap in knowledge about the extent, facies and stratigraphy of the Dachstein Carbonate Platform evolution in the Dinarides.

Assessing skeleton and microbiome responses of a calcareous sponge under thermal and pH stresses

Ocean higher temperature and acidity levels affect its carbonate chemistry, and calcifying organisms that depend on the calcium carbonate saturation state (ΩCaCO3) to build their skeleton may be vulnerable to these changes. Despite their important roles in the marine environment, little is known about the vulnerability of calcareous sponges under these stressors. We performed an acute short-term experiment (9 days) with thermal and pH stresses to explore their effects on the skeleton and microbiome of the calcareous sponge Sycettusa hastifera. We observed that sponge spicules showed no corrosion and no Mg/Ca ratio variation when exposed to stress conditions. However, the outermost spicules were smaller in low pH treatment, although these effects were often diminished when higher temperatures were also applied. In general, the sponges synthesized normally shaped spicules under stress conditions, but the proportion of deformed spicules increased significantly in elevated temperature. In addition, we observed a stable host–microbiome association in which there is microbiome flexibility under thermal and pH stresses with a significantly increase in abundance of some associated bacteria. Our results suggest that S. hastifera has low vulnerability under the future ocean conditions here designed, since it showed indications of resistance that could help them adapt and survive.

Temporal variation in the recruitment of calcareous sponges (Porifera, Calcarea) in Todos os Santos Bay, tropical Brazilian coast

Recruitment is related to the occupation of the substrate by fouling organisms. It plays an important role in the maintenance and distribution of benthic populations, being under the influence of biotic and abiotic factors. In the present work, the recruitment of calcareous sponges was monitored over two years in a marina at Todos os Santos Bay, a large bay in the tropical portion of the Brazilian coast. Artificial plates were immersed, being replaced bimonthly and the potential influence of the seawater temperature, photoperiod and precipitation on the number of sponge recruits was tested. The results showed that the number of calcareous sponge recruits had significant temporal variation. Nevertheless, different species showed different patterns over time. Significant differences were observed for Sycon avus, Sycon sp. and Leucandra serrata, and the periods with the highest number of recruits were different amongst them. Sycon bellum, Paraleucilla incomposita, Leucilla sp. and Heteropia glomerosa did not show significant variation in the number of recruits over time. None of the three tested environmental factors were correlated with the number of recruits, but results indicated S. avus recruitment might be driven by seawater temperature. Our results contribute to improve the current knowledge on the dynamics of each species found on the plates and reinforce the general view that the pattern of recruitment varies greatly in Calcarea, even amongst sympatric species.

Calcareous sponges from the French Polynesia (Porifera: Calcarea)

Although the French Polynesian reefs are among the most well studied reefs of the world, sponges are still poorly known, with only 199 species or OTUs of sponges having been described from French Polynesia, 167 at an OTU level and 32 at a species level. From those 199 species, just five are calcareous sponges. As it is possible that this number is underestimated, the aim of the present work was to study the diversity of calcareous sponges from French Polynesia. Hence, different French Polynesian archipelagos were surveyed by SCUBA from 3 to 60 m of depth. Identifications were performed using morphological and molecular (ITS and C-LSU) tools. We found a total of nine species of Calcarea, comprising five different genera. Five species are new to science: Clathrina fakaravae sp. nov., Clathrina huahineae sp. nov., Ernstia variabilis sp. nov., Leucascus digitiformis sp. nov., and Leucandra tahuatae sp. nov. With the present work, the number of identified sponges from French Polynesia at a species level increased from 32 to 41. The only calcareous sponge previously known from French Polynesia that was recollected by our group was Leucetta chagosensis. Our results suggest that the Eastern Indo-Pacific Realm shows more affinity with the Central and the Western Indo-Pacific Realms. Four species supported these affinities: Ascandra cf. crewsi, previously known only from Papua New Guinea, Leucascus simplex from South Australia, and Leucetta chagosensis and L. microraphis, both widespread species in the Indo-Pacific. These two Leucetta species, however, most likely represent species complexes. Once again the molecular markers ITS and C-LSU helped in the identification of calcareous sponges, showing how important is an integrative taxonomy. Although our work has increased in 250% (6 spp to 15 spp) the diversity of calcareous sponges in French Polynesia, it is most possible that this number is still underestimated.

Bioinspired synthesis of SnO crosses as backbone in artificial sponges

The distinct electronic properties, including p-type semiconducting and a wide optical band gap, renders SnO suitable for applications such as microelectronic devices, gas sensors and electrodes. However, the synthesis of SnO is rather challenging due to the instability of the oxide, which is usually obtained as a by-product of SnO 2 fabrication. In this work, we developed a bioinspired synthesis, based on a hydrothermal approach, for the direct production of SnO nanoparticles. The amount of mineralizer, inducing the precipitation, was identified, which supports a template-free formation of the nanosized SnO particles at low temperature and mild chemical conditions. Moreover, the SnO nanoparticles exhibit a shape of unique three-dimensional crosses similar to the calcite crosses present in the calcareous sponges. We demonstrated that SnO crosses are evenly distributed and embedded in an organic scaffold by an ice-templating approach, in this way closely mimicking the structure of calcareous sponges. Such scaffolds, reinforced by an active material, here SnO, could be used as filters, sensors or electrodes, where a high surface area and good accessibility are essential. This article is part of the theme issue ‘Bioinspired materials and surfaces for green science and technology (part 2)’.

Microbiota of the alien species Paraleucilla magna (Porifera, Calcarea) from the Southwestern Atlantic, and a comparison with that of other calcareous sponges

Sponges (Porifera) co-evolved with microorganisms in a well-established symbiotic relationship. Based on this characteristic, sponges can be separated into high microbial abundance (HMA) and low microbial abundance (LMA) species. Paraleucilla magna (Calcarea, Porifera) is an alien species of ecological importance in the Brazilian coastline. Little is known about the composition of its microbiota and that of other calcareous species, especially those inhabiting the Southwest Atlantic. Here, we describe the microbiota of P. magna and compare it to that of other calcareous sponge species for which such data exist. P. magna’s microbiota shows a lower diversity than that of Clathrina clathrus, C. coriacea, Leucosolenia sp., Leuconia sp. and Leucetta antarctica. P. magna microbiota is dominated by two bacterial OTUs of the Alphaproteobacteria class, that could not be classified beyond class (OTU001) and family levels (OTU002; Rhodospirillaceae). The Thaumarcheota was the predominant archaeal phylum in P. magna, with OTUs mainly affiliated to the genus candidatus Nitrosopumilus. The comparison with other calcareous species showed that microbiota composition correlated well with sponge phylogenetic affiliation. Metabolic prediction with PICRUSt software of P. magna bacterial microbiota indicated that membrane transport and carbohydrate, amino acid and energy metabolisms were most abundant while, for the archaeal domain, pathways related to translation, and energy metabolisms were predominant. Predicted metabolic features were compared between the different sponge species and seawater samples, showing that pathways related to cell motility, membrane transport, genetic information processing, xenobiotics metabolism and signal transduction are higher in the former while amino acid and nucleotide metabolism, translation, replication and repair, folding, sorting and degradation and glycan biosynthesis and metabolism are abundant in the latter. This study shows that P. magna’s microbiota is typical of an LMA sponge and that it differs from the microbiota of other calcareous sponges both in its composition and in predicted metabolic pathways.