Adapting to the Abyss: Passive Ventilation in the Deep-Sea Glass Sponge Euplectella aspergillum.

We analyze the flow physics inside the body cavity and downstream the deep-sea glass sponge Euplectella aspergillum. We provide evidence that the helical skeletal motifs of the sponge give rise to a rich fluid dynamic field, allowing the organism to scavenge flow from the bottom of the sea and promoting a spontaneous, organized vertical flow within its body cavity toward the osculum. Our analysis points at a functional adaptation of the organism, which can passively divert flow through the osculum in unfavorable, low ambient currents, with no need for active pumping, with potential repercussions in functional ecology, as well as the design of chemical reactors, air-treatment units, and civil and aeronaval structures.

Nested structure role in the mechanical response of spicule inspired fibers.

Euplectella aspergillummarine sponge spicules are renowned for their remarkable strength and toughness. These spicules exhibit a unique concentric layering structure, which contributes to their exceptional mechanical resistance. In this study, finite element method simulations were used to comprehensively investigate the effect of nested cylindrical structures on the mechanical properties of spicules. This investigation leveraged scanning electron microscopy images to guide the computational modeling of the microstructure and the results were validated by three-point bending tests of 3D-printed spicule-inspired structures. The numerical analyses showed that the nested structure of spicules induces stress and strain jumps on the layer interfaces, reducing the load on critical zones of the fiber and increasing its toughness. It was found that this effect shows a tapering enhancement as the number of layers increases, which combines with a threshold related to the 3D-printing manufacturability to suggest a compromise for optimal performance. A comprehensive evaluation of the mechanical properties of these fibers can assist in developing a new generation of bioinspired structures with practical real-world applications.

3D-printed bioinspired spicules: Strengthening and toughening via stereolithography.

Recently, the replication of biological microstructures has garnered significant attention due to their superior flexural strength and toughness, coupled with lightweight structures. Among the most intriguing biological microstructures renowned for their flexural strength are those found in the Euplectella Aspergillum (EA) marine sponges. The remarkable strength of this sponge is attributed to its complex microstructure, which consists of concentric cylindrical layers known as spicules with organic interlayers. These features effectively impede large crack propagation, imparting extraordinary mechanical properties. However, there have been limited studies aimed at mimicking the spicule microstructure. In this study, structures inspired by spicules were designed and fabricated using the stereolithography (SLA) 3D printing technique. The mechanical properties of concentric cylindrical structures (CCSs) inspired by the spicule microstructure were evaluated, considering factors such as the wall thickness of the cylinders, the number of layers, and core diameter, all of which significantly affect the mechanical response. These results were compared with those obtained from solid rods used as solid samples. The findings indicated that CCSs with five layers or fewer exhibited a flexural strength close to or higher than that of solid rods. Particularly, samples with 4 and 5 cylindrical layers displayed architecture similar to natural spicules. Moreover, in all CCSs, the absorbed energy was at least 3-4 times higher than solid rods. Conversely, CCSs with a cylinder wall thickness of 0.65 mm exhibited a more brittle behavior under the 3-point bending test than those with 0.35 mm and 0.5 mm wall thicknesses. CCSs demonstrated greater resistance to failure, displaying different crack propagation patterns and shear stress distributions under the bending test compared to solid rods. These results underscore that replicating the structure of spicules and producing structures with concentric cylindrical layers can transform a brittle structure into a more flexible one, particularly in load-bearing applications.

Cell cycle dynamics of food-entrapping cells of sponges: an experimental approach.

Sponges (phylum Porifera) exhibit surprisingly complex tissue dynamics, maintaining constant cell turnover and migration, rearranging internal structures, and regenerating after severe injuries. Such tissue plasticity relies on the activity of proliferating cells represented primarily by the food-entrapping cells, choanocytes. Although there are plenty of studies regarding the dynamics of regeneration and tissue rearrangement in sponges, cell cycle kinetics of choanocytes in intact tissues remains a controversial issue. This study is devoted to the comparative description of choanocyte cell cycle dynamics in intact tissues of two sponges, Halisarca dujardinii (class Demospongiae) and Leucosolenia corallorrhiza (class Calcarea). We have identified populations of proliferating cells and synchronized them in the S-phase to estimate the growth fraction of cycling cells. Using continuous exposure to labeled thymidine analog ethynyl deoxyuridine (EdU), we calculated choanocyte cell cycle duration and the length of the S phase. We also applied double labeling with EdU and antibodies against phosphorylated histone 3 to estimate the lengths of choanocyte M and G2 phases. Finally, flow-cytometry-based quantitative analysis of DNA content provided us with the lengths of G2 and G1 phases. We found that tissue growth and renewal in the studied sponges are generally maintained by a relatively large population of slowly cycling choanocytes with a total cell cycle duration of 40 h in H. dujardinii and 60 h in L. corallorrhiza. In both species, choanocytes are characterized by an extremely short M-phase and heterogeneity in the duration of the G2 phase.

Anthracene and Pyrene Biodegradation Performance of Marine Sponge Symbiont Bacteria Consortium.

Every petroleum-processing plant produces sewage sludge containing several types of polycyclic aromatic hydrocarbons (PAHs). The degradation of PAHs via physical, biological, and chemical methods is not yet efficient. Among biological methods, the use of marine sponge symbiont bacteria is considered an alternative and promising approach in the degradation of and reduction in PAHs. This study aimed to explore the potential performance of a consortium of sponge symbiont bacteria in degrading anthracene and pyrene. Three bacterial species (Bacillus pumilus strain GLB197, Pseudomonas stutzeri strain SLG510A3-8, and Acinetobacter calcoaceticus strain SLCDA 976) were mixed to form the consortium. The interaction between the bacterial consortium suspension and PAH components was measured at 5 day intervals for 25 days. The biodegradation performance of bacteria on PAH samples was determined on the basis of five biodegradation parameters. The analysis results showed a decrease in the concentration of anthracene (21.89%) and pyrene (7.71%), equivalent to a ratio of 3:1, followed by a decrease in the abundance of anthracene (60.30%) and pyrene (27.52%), equivalent to a ratio of 2:1. The level of pyrene degradation was lower than that of the anthracene due to fact that pyrene is more toxic and has a more stable molecular structure, which hinders its metabolism by bacterial cells. The products from the biodegradation of the two PAHs are alcohols, aldehydes, carboxylic acids, and a small proportion of aromatic hydrocarbon components.

Snails associated with the coral-killing sponge Terpios hoshinota in Okinawa Island, Japan.

Terpios hoshinota is a thin encrusting sponge that overgrows live scleractinian corals and it is linked to coral loss in many reefs. However, our knowledge of the species associated with this sponge species is poor. During a periodical survey of T. hoshinota in 2020, we found tiny snails crawling on the sponge in the subtropical waters around Okinawa Island, Japan. We observed egg capsules inside the sponge tissue and veliger larvae released from the egg capsules. Molecular analyses of both the snails and veliger larvae (cytochrome oxidase I, COI) showed that they were identical and belonged to Joculator sp. (family Cerithiopsidae). There was no direct observation of predation on the sponge by this snail; however, to the best of our knowledge, this is the first report on a close association between a snail and the sponge T. hoshinota.

Extreme flow simulations reveal skeletal adaptations of deep-sea sponges.

Since its discovery1,2, the deep-sea glass sponge Euplectella aspergillum has attracted interest in its mechanical properties and beauty. Its skeletal system is composed of amorphous hydrated silica and is arranged in a highly regular and hierarchical cylindrical lattice that begets exceptional flexibility and resilience to damage3-6. Structural analyses dominate the literature, but hydrodynamic fields that surround and penetrate the sponge have remained largely unexplored. Here we address an unanswered question: whether, besides improving its mechanical properties, the skeletal motifs of E. aspergillum underlie the optimization of the flow physics within and beyond its body cavity. We use extreme flow simulations based on the 'lattice Boltzmann' method7, featuring over fifty billion grid points and spanning four spatial decades. These in silico experiments reproduce the hydrodynamic conditions on the deep-sea floor where E. aspergillum lives8-10. Our results indicate that the skeletal motifs reduce the overall hydrodynamic stress and support coherent internal recirculation patterns at low flow velocity. These patterns are arguably beneficial to the organism for selective filter feeding and sexual reproduction11,12. The present study reveals mechanisms of extraordinary adaptation to live in the abyss, paving the way towards further studies of this type at the intersection between fluid mechanics, organism biology and functional ecology.

Expression of Wnt and TGF-Beta Pathway Components during Whole-Body Regeneration from Cell Aggregates in Demosponge Halisarca dujardinii.

The phenomenon of whole-body regeneration means rebuilding of the whole body of an animal from a small fragment or even a group of cells. In this process, the old axial relationships are often lost, and new ones are established. An amazing model for studying this process is sponges, some of which are able to regenerate into a definitive organism after dissociation into cells. We hypothesized that during the development of cell aggregates, primmorphs, new axes are established due to the activation of the Wnt and TGF-beta signaling pathways. Using in silico analysis, RNA-seq, and whole-mount in situ hybridization, we identified the participants in these signaling pathways and determined the spatiotemporal changes in their expression in demosponge Halisarca dujardinii. It was shown that Wnt and TGF-beta ligands are differentially expressed during primmorph development, and transcripts of several genes are localized at the poles of primmorphs, in the form of a gradient. We suppose that the Wnt and TGF-beta signaling cascades are involved in the initial axial patterning of the sponge body, which develops from cells after dissociation.

Whole-Body Regeneration in Sponges: Diversity, Fine Mechanisms, and Future Prospects.

While virtually all animals show certain abilities for regeneration after an injury, these abilities vary greatly among metazoans. Porifera (Sponges) is basal metazoans characterized by a wide variety of different regenerative processes, including whole-body regeneration (WBR). Considering phylogenetic position and unique body organization, sponges are highly promising models, as they can shed light on the origin and early evolution of regeneration in general and WBR in particular. The present review summarizes available data on the morphogenetic and cellular mechanisms accompanying different types of WBR in sponges. Sponges show a high diversity of WBR, which principally could be divided into (1) WBR from a body fragment and (2) WBR by aggregation of dissociated cells. Sponges belonging to different phylogenetic clades and even to different species and/or differing in the anatomical structure undergo different morphogeneses after similar operations. A common characteristic feature of WBR in sponges is the instability of the main body axis: a change of the organism polarity is described during all types of WBR. The cellular mechanisms of WBR are different across sponge classes, while cell dedifferentiations and transdifferentiations are involved in regeneration processes in all sponges. Data considering molecular regulation of WBR in sponges are extremely scarce. However, the possibility to achieve various types of WBR ensured by common morphogenetic and cellular basis in a single species makes sponges highly accessible for future comprehensive physiological, biochemical, and molecular studies of regeneration processes.

Testing of how and why the Terpios hoshinota sponge kills stony corals.

An encrusting sponge, Terpios hoshinota, has the potential to infect all species of stony corals in shallow reefs and killing them. It caused a decline in coral coverage in two south-eastern islands of Taiwan. We proposed two hypotheses to examine how the sponges kill the corals, namely, light blocking and toxins, and tested by in-situ experiments. The results revealed that both light blocking, sponge toxins, and particularly the combination of both factors were effective at inducing tissue damage in stony corals over a short period. Second, to answer why the sponges killed the corals, we tested two hypotheses, namely, gaining nutrients versus gaining substrates for the sponge. By analyzing the stable isotopes 13C and 15N, as well as exploiting an enrichment experiment, it was possible to determine that only approximately 9.5% of the carbon and 16.9% of the nitrogen in the newly grown sponge tissues originated from the enriched corals underneath. The analysis also revealed that the control corals without isotope enrichment had higher δ13C and δ15N than the control sponges, which was an additional indication that T. hoshinota did not rely heavily on corals for nutrients. Therefore, our results support the hypothesis that the encrusting sponge did not kill corals for food or nutrients, but rather for the substrate.

In situ observation of sponge trails suggests common sponge locomotion in the deep central Arctic.

In 2016, the research ice-breaker Polarstern surveyed the submerged peaks of the permanently ice-covered Langseth Ridge, a tectonic feature comprising the Karasik seamount and two deeper seamount peaks, abutting the Gakkel ultra-slow spreading ridge (87°N 62°E to 85.5°N 57.4°E)1. A towed marine camera sled and a hybrid remotely operated vehicle revealed these peaks to be covered by a dense demosponge community, at first glance reminiscent of North Atlantic Geodia grounds (sensu2). Sponges were observed on top of a thick layer of spicule mat (Figure 1 and Video S1), intermixed with underlying layers of empty siboglinid tubes and bivalve shells, a substrate covering almost the entire seafloor. We observed trails of densely interwoven spicules connected directly to the underside or lower flanks of sponge individuals (Figure 1), suggesting these trails are traces of motile sponges. This is the first time abundant sponge trails have been observed in situ and attributed to sponge mobility. Given the low primary production in this permanently ice-covered region, these trails may relate to feeding behavior and/or a strategy for dispersal of juveniles. Such trails may remain visible for long periods given the regionally low sedimentation rates.

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland.

Climate change is expanding marine oxygen minimum zones (OMZs), while anthropogenic nutrient input depletes oxygen concentrations locally. The effects of deoxygenation on animals are generally detrimental; however, some sponges (Porifera) exhibit hypoxic and anoxic tolerance through currently unknown mechanisms. Sponges harbor highly specific microbiomes, which can include microbes with anaerobic capabilities. Sponge-microbe symbioses must also have persisted through multiple anoxic/hypoxic periods throughout Earth's history. Since sponges lack key components of the hypoxia-inducible factor (HIF) pathway responsible for hypoxic responses in other animals, it was hypothesized that sponge tolerance to deoxygenation may be facilitated by its microbiome. To test this hypothesis, we determined the microbial composition of sponge species tolerating seasonal anoxia and hypoxia in situ in a semienclosed marine lake, using 16S rRNA amplicon sequencing. We discovered a high degree of cryptic diversity among sponge species tolerating seasonal deoxygenation, including at least nine encrusting species of the orders Axinellida and Poecilosclerida. Despite significant changes in microbial community structure in the water, sponge microbiomes were species specific and remarkably stable under varied oxygen conditions, which was further explored for Eurypon spp. 2 and Hymeraphia stellifera However, some symbiont sharing occurred under anoxia. At least three symbiont combinations, all including large populations of Thaumarchaeota, corresponded with deoxygenation tolerance, and some combinations were shared between some distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance.IMPORTANCE The oceans have an uncertain future due to anthropogenic stressors and an uncertain past that is becoming clearer with advances in biogeochemistry. Both past and future oceans were, or will be, deoxygenated in comparison to present conditions. Studying how sponges and their associated microbes tolerate deoxygenation provides insights into future marine ecosystems. Moreover, sponges form the earliest branch of the animal evolutionary tree, and they likely resemble some of the first animals. We determined the effects of variable environmental oxygen concentrations on the microbial communities of several demosponge species during seasonal anoxia in the field. Our results indicate that anoxic tolerance in some sponges may depend on their symbionts, but anoxic tolerance was not universal in sponges. Therefore, some sponge species could likely outcompete benthic organisms like corals in future, reduced-oxygen ecosystems. Our results support the molecular evidence that sponges and other animals have a Neoproterozoic origin and that animal evolution was not limited by low-oxygen conditions.

Reafference and the origin of the self in early nervous system evolution.

Discussions of the function of early nervous systems usually focus on a causal flow from sensors to effectors, by which an animal coordinates its actions with exogenous changes in its environment. We propose, instead, that much early sensing was reafferent; it was responsive to the consequences of the animal's own actions. We distinguish two general categories of reafference-translocational and deformational-and use these to survey the distribution of several often-neglected forms of sensing, including gravity sensing, flow sensing and proprioception. We discuss sensing of these kinds in sponges, ctenophores, placozoans, cnidarians and bilaterians. Reafference is ubiquitous, as ongoing action, especially whole-body motility, will almost inevitably influence the senses. Corollary discharge-a pathway or circuit by which an animal tracks its own actions and their reafferent consequences-is not a necessary feature of reafferent sensing but a later-evolving mechanism. We also argue for the importance of reafferent sensing to the evolution of the body-self, a form of organization that enables an animal to sense and act as a single unit. This article is part of the theme issue 'Basal cognition: multicellularity, neurons and the cognitive lens'.

Cytotoxic Alkaloids Derived from Marine Sponges: A Comprehensive Review.

Marine sponges (porifera) have proved to be a prolific source of unique bioactive secondary metabolites, among which the alkaloids occupy a special place in terms of unprecedented structures and outstanding biological activities. Identification of active cytotoxic alkaloids extracted from marine animals, particularly sponges, is an important strive, due to lack of knowledge on traditional experiential and ethnopharmacology investigations. In this report, a comprehensive survey of demospongian bioactive alkaloids in the range 1987-2020 had been performed with a special emphasis on the potent cytotoxic activity. Different resources and databases had been investigated, including Scifinder (database for the chemical literature) CAS (Chemical Abstract Service) search, web of science, Marin Lit (marine natural products research) database. More than 230 representatives of different classes of alkaloids had been reviewed and classified, different genera belonging to the phylum porifera had been shown to be a prolific source of alkaloidal molecules, including Agelas sp., Suberea sp., Mycale sp., Haliclona sp., Epipolasis sp., Monanchora sp., Crambe sp., Reniera sp., and Xestospongia sp., among others. The sufficient production of alkaloids derived from sponges is a prosperous approach that requires more attention in future studies to consider the constraints regarding the supply of drugs, attained from marine organisms.

Hydrodynamics of sponge pumps and evolution of the sponge body plan.

Sponges are suspension feeders that filter vast amounts of water. Pumping is carried out by flagellated chambers that are connected to an inhalant and exhalant canal system. In 'leucon' sponges with relatively high-pressure resistance due to a complex and narrow canal system, pumping and filtering are only possible owing to the presence of a gasket-like structure (forming a canopy above the collar filters). Here, we combine numerical and experimental work and demonstrate how sponges that lack such sealing elements are able to efficiently pump and force the flagella-driven flow through their collar filter, thanks to the formation of a 'hydrodynamic gasket' above the collar. Our findings link the architecture of flagellated chambers to that of the canal system, and lend support to the current view that the sponge aquiferous system evolved from an open-type filtration system, and that the first metazoans were filter feeders.

Spatial patterns of continental shelf faunal community structure along the Western Antarctic Peninsula.

Knowledge of continental shelf faunal biodiversity of Antarctica is patchy and as such, the ecology of this unique ecosystem is not fully understood. To this end, we deployed baited cameras at 20 locations along ~ 500 km of the Western Antarctic Peninsula (WAP) at depths from 90 to 797 m. We identified 111 unique taxa, with mud bottom accounting for 90% of the dominant (≥ 50% cover) habitat sampled. Amphipoda comprised 41% of the total maximum number of individuals per camera deployment (MaxN) and occurred on 75% of deployments. Excluding this taxon, the highest MaxN occurred around King George/25 de Mayo Island and was driven primarily by the abundance of krill (Euphausiidae), which accounted for 36% of total average MaxN among deployments around this island. In comparison, krill comprised 22% of total average MaxN at Deception Island and only 10% along the peninsula. Taxa richness, diversity, and evenness all increased with depth and depth explained 18.2% of the variation in community structure among locations, which may be explained by decreasing ice scour with depth. We identified a number of Vulnerable Marine Ecosystem taxa, including habitat-forming species of cold-water corals and sponge fields. Channichthyidae was the most common fish family, occurring on 80% of all deployments. The Antarctic jonasfish (Notolepis coatsorum) was the most frequently encountered fish taxa, occurring on 70% of all deployments and comprising 25% of total MaxN among all deployments. Nototheniidae was the most numerically abundant fish family, accounting for 36% of total MaxN and was present on 70% of the deployments. The WAP is among the fastest warming regions on Earth and mitigating the impacts of warming, along with more direct impacts such as those from fishing, is critical in providing opportunities for species to adapt to environmental change and to preserve this unique ecosystem.

Transmission of the sponge microbiome: moving towards a unified model.

Sponges have co-evolved for millions of years alongside several types of microorganisms, which aside from participating in the animal's diet, are mostly symbionts. Since most of the genetic repertoire in the holobiont genome is provided by microbes, it is expected that the host-associated microbiome will be at least partially heritable. Sponges can therefore acquire their symbionts in different ways. Both vertical transmission (VT) and horizontal transmission (HT) have different advantages and disadvantages in the life cycle of these invertebrates. However, a third mode of transmission, called leaky vertical transmission or mixed mode of transmission (MMT), which incorporates both VT and HT modes, has gained relevance and seems to be the most robust model. In that regard, the aim of this review is to present the evolving knowledge on these main modes of transmission of the sponge microbiome. Our conclusions lead us to suggest that MMT may be more common for all sponges, with its frequency varying across the transmission spectrum between species and the environment. This hybrid model supports the stable and specific transmission of these microbial partners and reinforces their assistance in the resilience of sponges over the years.

Cross-generational effects of climate change on the microbiome of a photosynthetic sponge.

Coral reefs are facing increasing pressure from rising seawater temperatures and ocean acidification. Sponges have been proposed as possible winners in the face of climate change; however, little is known about the mechanisms underpinning their predicted tolerance. Here we assessed whether microbiome-mediated cross-generational acclimatization could enable the photosynthetic sponge Carteriospongia foliascens to survive under future climate scenarios. To achieve this, we first established the potential for vertical (cross-generational) transmission of symbionts. Sixty-four amplicon sequence variants accounting for >90% of the total C. foliascens microbial community were present across adult, larval and juvenile life stages, showing that a large proportion of the microbiome is vertically acquired and maintained. When C. foliascens were exposed to climate scenarios projected for 2050 and 2100, the host remained visibly unaffected (i.e. no necrosis/bleaching) and the overall microbiome was not significantly different amongst treatments in adult tissue, the respective larvae or recruits transplanted amongst climate treatments. However, indicator species analysis revealed that parental exposure to future climate scenarios altered the presence and abundance of a small suite of microbial taxa in the recruits, thereby revealing the potential for microbiome-mediated cross-generational acclimatization through both symbiont shuffling and symbiont switching within a vertically acquired microbiome.

Molecular Network and Culture Media Variation Reveal a Complex Metabolic Profile in Pantoea cf. eucrina D2 Associated with an Acidified Marine Sponge.

The Gram-negative Pantoea eucrina D2 was isolated from the marine sponge Chondrosia reniformis. Sponges were collected in a shallow volcanic vents system in Ischia island (South Italy), influenced by CO2 emissions and lowered pH. The chemical diversity of the secondary metabolites produced by this strain, under different culture conditions, was explored by a combined approach including molecular networking, pure compound isolation and NMR spectroscopy. The metabolome of Pantoea cf. eucrina D2 yielded a very complex molecular network, allowing the annotation of several metabolites, among them two biosurfactant clusters: lipoamino acids and surfactins. The production of each class of metabolites was highly dependent on the culture conditions, in particular, the production of unusual surfactins derivatives was reported for the first time from this genus; interestingly the production of these metabolites only arises by utilizing inorganic nitrogen as a sole nitrogen source. Major components of the extract obtained under standard medium culture conditions were isolated and identified as N-lipoamino acids by a combination of 1D and 2D NMR spectroscopy and HRESI-MS analysis. Assessment of the antimicrobial activity of the pure compounds towards some human pathogens, indicated a moderate activity of leucine containing N-lipoamino acids towards Staphylococcus aureus, Staphylococcus epidermidis and a clinical isolate of the emerging food pathogen Listeria monocytogenes.

Soaking up the oil: Biological impacts of dispersants and crude oil on the sponge Halichondria panicea.

Used during an oil spill to minimise the formation of an oil slick, dispersants have negative biological effects on marine model organisms. However, no study has investigated the impacts of dispersants on adult sponge individuals. Here, we examine the effects of water accommodated oil fraction (WAF - oil in seawater), chemically enhanced WAF (CEWAF - oil and dispersant in seawater) and Benzo[A]Pyrene on sponge Halichondria panicea at physiological and molecular levels. Sponge clearance rate decreased sharply when exposed to WAF and CEWAF but the oil loading at which the clearance rate was reduced by 50% (ED50) was 39-fold lower in CEWAF than in WAF. Transcriptomic analysis revealed a homogenous molecular response with the greatest number of differentially expressed genes identified in CEWAF samples (1,461 genes). Specifically, genes involved in stress responses were up-regulated. This study presents evidence that the use of dispersants should be considered carefully in areas where sponges are present.