Sponge Larvae Research Articles

Outer membrane vesicles from commensal microbes contribute to the sponge Tedania sp. development by regulating the expression level of apoptosis-inducing factor (AIF)

The transition from the swimming larval stage to the settlement stage represents a significant node in the marine sponge developmental process. Previous research has shown that the outer membrane vesicles (OMVs) from the bacterial species Tenacibaculum mesophilum associated with the sponge Tedania sp. influence larval settlement: low concentrations of OMVs increase the attachment rate, whereas high concentrations decrease the attachment rate. Here, by comparing the transcriptomes of sponge larvae in filtered seawater (FSW group) and in FSW supplemented with OMVs (FSW-OMV group), the results indicated that bacterial OMVs affected larval settlement by modulating the expression levels of apoptosis-inducing factor (AIF) in the host. Subsequently, quantitative real-time PCR revealed a decrease in aif expression near the time of settlement (SE) compared to that in the control group. RNA interference (RNAi) was used to target the aif gene, and the rate of larval settlement was significantly reduced, confirming the inhibitory effect of high concentrations of OMVs. Moreover, small RNA (sRNA) sequencing of OMVs revealed the existence of abundant AIF-sRNAs of 30 nt, further suggesting that one pathway for the involvement of sponge-associated bacteria in host development is the transport of OMVs and the direct function of cargo loading.

Multiomics integration for the function of bacterial outer membrane vesicles in the larval settlement of marine sponges.

Bacterial outer membrane vesicles (OMVs) contain a variety of chemical compounds and play significant roles in maintaining symbiotic relationships in a changing ocean, but little is known about their function, particularly in sponge larval development. During the growth of sponge Tedania sp., OMVs from Bacteroidetes species significantly promoted larval settlement, and Tenacibaculum mesophilum SP-7-OMVs were selected as a representative strain for further investigation. According to OMVs metabolomics, larval settlement might be connected to organic acids and derivatives. The multiomics analysis of the T. mesophilum genome, SP-7-OMVs metabolome, and larval transcriptome revealed 47 shared KEGG pathways. Among the number of candidate metabolites, arginine was chosen for its greater ability to increase the settlement rate and its role as the principal substrate for nitric oxide (NO) synthesis of sponge larvae. In summary, these results demonstrated that sponge-associated bacteria might utilize OMVs and their cargo to support host development and make up for host metabolic pathway deficiencies. This study enhances our fundamental knowledge of OMVs in interactions between metazoan hosts and microorganisms that are crucial in the coevolution of marine ecosystems and the complex marine environment.

Molecular responses of sponge larvae exposed to partially weathered condensate oil

Anthropogenic inputs of petroleum hydrocarbons into the marine environment can have long lasting impacts on benthic communities. Sponges form an abundant and diverse component of benthic habitats, contributing a variety of important functional roles; however, their responses to petroleum hydrocarbons are largely unknown. This study combined a traditional ecotoxicological experimental design and endpoint with global gene expression profiling and microbial indicator species analysis to examine the effects of a water accommodated fraction (WAF) of condensate oil on a common Indo-Pacific sponge, Phyllospongia foliascens. A no significant effect concentration (N(S)EC) of 2.1 % WAF was obtained for larval settlement, while gene-specific (N(S)EC) thresholds ranged from 3.4 % to 8.8 % WAF. Significant shifts in global gene expression were identified at WAF treatments ≥20 %, with larvae exposed to 100 % WAF most responsive. Results from this study provide an example on the incorporation of non-conventional molecular and microbiological responses into ecotoxicological studies on petroleum hydrocarbons.

Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica.

Interkingdom signalling within a holobiont allows host and symbionts to communicate and to regulate each other's physiological and developmental states. Here we show that a suite of signalling molecules that function as neurotransmitters and neuromodulators in most animals with nervous systems, specifically dopamine and trace amines, are produced exclusively by the bacterial symbionts of the demosponge Amphimedon queenslandica. Although sponges do not possess a nervous system, A. queenslandica expresses rhodopsin class G-protein-coupled receptors that are structurally similar to dopamine and trace amine receptors. When sponge larvae, which express these receptors, are exposed to agonists and antagonists of bilaterian dopamine and trace amine receptors, we observe marked changes in larval phototactic swimming behaviour, consistent with the sponge being competent to recognise and respond to symbiont-derived trace amine signals. These results indicate that monoamines synthesised by bacterial symbionts may be able to influence the physiology of the host sponge.

Marine heatwave conditions drive carryover effects in a temperate sponge microbiome and developmental performance.

Marine heatwaves are increasingly subjecting organisms to unprecedented stressful conditions, but the biological consequences of these events are still poorly understood. Here we experimentally tested the presence of carryover effects of heatwave conditions on the larval microbiome, settlers growth rate and metamorphosis duration of the temperate sponge Crella incrustans. The microbial community of adult sponges changed significantly after ten days at 21°C. There was a relative decrease in symbiotic bacteria, and an increase in stress-associated bacteria. Sponge larvae derived from control sponges were mainly characterised by a few bacterial taxa also abundant in adults, confirming the occurrence of vertical transmission. The microbial community of sponge larvae derived from heatwave-exposed sponges showed significant increase in the endosymbiotic bacteria Rubritalea marina. Settlers derived from heatwave-exposed sponges had a greater growth rate under prolonged heatwave conditions (20 days at 21°C) compared to settlers derived from control sponges exposed to the same conditions. Moreover, settler metamorphosis was significantly delayed at 21°C. These results show, for the first time, the occurrence of heatwave-induced carryover effects across life-stages in sponges and highlight the potential role of selective vertical transmission of microbes in sponge resilience to extreme thermal events.

Effects of ocean acidification on the early life history processes of the breadcrumb sponge Halichondria panicea

AbstractOcean acidification (OA) is predicted to result in reduced survival, growth, reproduction, and overall biodiversity of marine invertebrates, and yet we lack information about the response to OA of some major groups of marine organisms. In particular, we know relatively little about how OA will impact temperate sponges, which will experience more extreme low pH conditions than tropical species. In this study, we quantified OA‐induced changes in early life history patterns (larval mortality and condition, settlement rate, recruit survival, and size) in the non‐calcifying breadcrumb sponge Halichondria panicea collected from a temperate intertidal site in the California Current Large Marine Ecosystem. Sponge larvae were exposed to OA conditions for 15 days, and early life history patterns were observed. Compared with baseline (“present”) conditions, larval mortality and settlement rates increased in the acidified treatment (“future”). This effect was restricted to larval stages; treatment had no effect on the growth and survival of recruits. This study is significant in that it shows that H. panicea may be particularly vulnerable to changes in ocean pH during the larval stage, which could ultimately reduce total sponge abundance by diminishing the number of larvae that survive to settlement.

Life in the Fast Lane: Modeling the Fate of Glass Sponge Larvae in the Gulf Stream

Effective conservation management of deep-sea sponges, including design of appropriate marine protected areas, requires an understanding of the connectivity between populations throughout a species’ distribution. We provide the first consideration of larval connectivity among deep-sea sponge populations along the southeastern coast of North America, illustrate the influence of the Gulf Stream on dispersal, and complement published distribution models by evaluating colonization potential. Connectivity among known populations of the hexactinellid sponge Vazella pourtalesii was simulated using a 3-D biophysical dispersal model throughout its distribution from Florida, United States to Nova Scotia, Canada. We found no exchange with an estimated pelagic larval duration of 2 weeks between populations north and south of Cape Hatteras, North Carolina at surface, mid-water and seabed release depths, irrespective of month of release or application of a horizontal diffusion constant specific to cross-Gulf Stream diffusivity. The population north of Cape Hatteras and south of Cape Cod was isolated. There was some evidence that Gulf Stream eddies formed near Cape Hatteras could travel to the northwest, connecting the populations in the two sub-regions, however that would require a much longer pelagic duration than what is currently known. More likely almost all larval settlement will be in the immediate area of the adults. At sub-regional scales, connectivity was found from the Strait of Florida through to the Blake Plateau, southeastern United States, with the latter area showing potential for recruitment from more than one source population. The influence of the Charleston Bump, a shallow feature rising from the Blake Plateau, was substantial. Particles seeded just north of the Bump were transported greater distances than those seeded to the south, some of which were caught in an associated gyre, promoting retention at the seabed. To the north on the Scotian Shelf, despite weaker currents and greater distances between known occurrences, unidirectional transport was detected from Emerald Basin to the Northeast Channel between Georges and Browns Banks. These major conclusions remained consistent through simulations run with different averaging periods for the currents (decades to daily) and using two ocean model products (BNAM and GLORYS12V1).

Derivation of toxicity thresholds for gas condensate oils protective of tropical species using experimental and modelling approaches

Toxicity thresholds for dissolved oil applied in tropical ocean risk assessments are largely based on the sensitivities of temperate and/or freshwater species. To explore the suitability of these thresholds for tropical habitats we experimentally determined toxicity thresholds for eight tropical species for a partially weathered gas condensate, applied the target lipid model (TLM) to predict toxicity of fresh and weathered condensates and compared sensitivities of the tropical species with model predictions. The experimental condensate-specific hazard concentration (HC5) was 167 μg L−1 total aromatic hydrocarbons (TAH), with the TLM-modelled HC5 (78 μg L−1 TAH) being more conservative, supporting TLM-modelled thresholds for tropical application. Putative species-specific critical target lipid body burdens (CTLBBs) indicated that several of the species tested were among the more sensitive species in the TLM database ranging from 5.1 (coral larvae) to 97 (sponge larvae) μmol g−1 octanol and can be applied in modelling risk for tropical marine ecosystems.

Dopamine-like immunoreactivity in sponge larvae

Dopamine-like immunoreactivity in sponge larvae

Bacteroidetes bacteria, important players in the marine sponge larval development process

SummaryBacteroidetes bacteria are frequently found in association with sponges, but their roles in host development are poorly understood. In this study, thirteen bacterial species (12 genera) isolated from the sponge Tedania sp. revealed a common ability to significantly promote sponge larval settlement at rates 30.00–53.33% higher than controls (p < 0.05). Three effective strategies were adapted: (i) two strains formed biofilms enhancing the settlement rate to 56.67–63.33% within three days. (ii) Five strains secreted hydrosoluble molecules improving larval settlement, reaching 59.17%. (iii) Six species produced extracellular vesicles (EVs) that significantly improved settlement by up to 86.67% (p < 0.05). The EV fluorescence demonstrated that they migrated inside the sponge larvae from the planktonic to metamorphosis stage. Generally, marine sponges specifically enrich Bacteroidetes bacteria because of the important player in host development, establishing the basis for reciprocal adaptive co-evolution between the microbial community and animals, even including higher organisms.

The kinetid structure of two oscarellid sponges (Class Homoscleromorpha) unveils plesiomorphies in kinetids of Homoscleromorpha–Calcarea lineage

AbstractThe structure of the kinetid (flagellar or ciliary apparatus) is known to be of phylogenetic significance in sponges (Phylum Porifera) and can provide information about evolutionary relationships. Here, we report on the larval kinetid structure of two closely related species, Oscarella lobularis and O. tuberculata (Homoscleromorpha, Oscarellidae). Cells belonging to the four previously recognized morphological regions (anterior pole, lateral zone, paracrystalline belt, and posterior pole) were studied. The cells of the paracrystalline belt have pear‐shaped nuclei with a paracrystalline inclusion connected to the roots of the kinetid. In the cells of other zones, the nucleus is separated from the kinetid, and the roots adjoined the Golgi apparatus only. In kinetids of the studied larval cells, we observed the accessory centriole arranged immediately under the kinetosome, and two unequal fibrillar roots. These features are unique for sponge larvae. Comparing kinetids of the Homoscleromorpha with those in its sister group, the Calcarea, we propose an ancestral composition for the kinetid in the lineage Calcarea + Homoscleromorpha. This proposed kinetid structure includes a kinetosome–nucleus link, striated roots, simple basal foot, orthogonal centriole, and a long transition zone of the flagellum. The position of the centriole under the kinetosome in homoscleromorph larvae and the stout fibrillar or microtubular bundle on the kinetosome in calcarean larvae might be the apomorphies of these groups.

Kinetid in larval cells of Spongillida (Porifera: Demospongiae): tracing the ancestral traits

The kinetid (flagellar/ciliary apparatus) of eukaryotic cells is an important source of phylogenetic information. It was found to be a prospective morphological phylogenetic marker in sponges, since its arrangement in choanocytes is congruent with the topology of the phylogenetic trees. However, investigation of the kinetid of sponge larval cells remains fragmentary. Here, we report the results of an ultrastructural study on the larval kinetids of the freshwater sponges Eunapius fragilis and Lubomirskia baikalensis (Demospongiae: Spongillida). Their kinetids were found to comprise a kinetosome associated with an accessory centriole and linked to the nucleus by a simple fibrillar root. The kinetosome bears a transverse cytoskeleton: filamentous train and microtubules which radiate from a microtubule organising centre (MTOC) shaped as a large hollow foot. In the short transition zone, between the central axonemal microtubules and kinetosome, a transverse plate with an axosome (central thickening) occurs. We have reviewed the kinetids of different sponge larvae to reconstruct the ancestral state of these traits. Thus, we suggest that spongillids retain the plesiomorphic characteristics of roots and an accessory centriole. But they possess the peculiarities of the transition zone, transverse cytoskeleton and MTOC structure.

Cultivation of sponge Haliclona simulans juveniles in a floating sea raft

Large-scale mariculture of a marine sponge requires a sustainable seed stock that can be raised artificially. To find the optimized breeding methods for Haliclona simulans juveniles, a study with three stages, starting from free swimming larvae, was performed in a field laboratory placed on a floating sea raft. In the first step, six different substrates were compared, and polystyrene plastic petri dishes were found to be the optimal substrates for settlement and metamorphosis of H. simulans swimming larvae. Then, in the second stage, 30-days growth experiments with 20 conditions were performed for the larvae settled on plastic petri dishes. The optimized devices and conditions suited for the early-stage cultivation of sponge larvae were obtained. In the final stage, a 4-months growth experiment was performed with the guidance of the optimized conditions acquired from the former stages. At the end of the experiment, the group with the highest growth rate achieved an average length of 18.44 ± 10.73 mm, and the largest juvenile length reached 33.4 mm, equivalent to a 45-folds increase in length or over 20,000-folds increase in volume when compared to the larvae that just settled. Thus, we established a feasible and low-cost sponge-larval mariculture pattern, upon which the culturing procedures can be improved and the sustainable seed stock needed for sponge large-scale culture becomes possible.

Sponge larvae are not that fast, but still the fastest

Sponge larvae are not that fast, but still the fastest

Settlement of juvenile glass sponges and other invertebrate cryptofauna on the Hecate Strait glass sponge reefs

AbstractGlass sponge reefs are endemic to the continental shelf waters of British Columbia and Alaska, where they form complex three‐dimensional habitats used by a variety of commercially important fish and invertebrate species. The Hecate Strait and Queen Charlotte Sound Glass Sponge Reefs Marine Protected Area (HSQCS‐MPA) was designated in February 2017 to protect 2,410 km2 of reef habitat. Efforts to establish baseline information regarding reef‐associated taxa in the new MPA have documented the diversity of megafauna in detail, but little is understood of the cryptic epifauna inhabiting hidden crevices within the reefs, and even less is understood of larval recruitment, the key reproductive process maintaining long‐term reef health and stability. We collected specimens of a reef‐building glass sponge, Farrea occa, from the HSQCS‐MPA and described the diversity of their epifauna. Five hundred and two organisms from six phyla were documented, including 84 sponges from three classes. We found several glass sponges: known juvenile reef builders (two Aphrocallistes vastus and two Heterochone calyx); the lyssacine sponge Leucopsacus scoliodocus, previously known in Canadian waters only from Jervis Inlet; and an unidentified dictyonine sponge previously unknown to waters of British Columbia. Also present were the carnivorous sponge Lycopodina occidentalis, 11 individuals of Desmacella austini, evidence for a new species in the subgenus Haliclona (Flagellia), and a clathrinid calcareous sponge. The growth stages we observed suggest multiple settlement events by glass sponge larvae between February and early March. Of the 502 invertebrates, 460 were attached to dead sponge skeleton despite live tissue being much more available as substrate. This study highlights trends in recruitment at sponge reefs, explores factors that may affect larval settlement, describes new sponge associations, and provides the first description of the range of macrofauna found on glass sponges, acting as a baseline for continued monitoring of the MPA.

Sponge larvae do not swim that fast: a reply to Montgomery et al. (2019)

Sponge larvae do not swim that fast: a reply to Montgomery <i>et al</i>. (2019)

Immediate Effects of Hurricanes on a Diverse Coral/Mangrove Ecosystem in the U.S. Virgin Islands and the Potential for Recovery

Hurricanes Irma and Maria, two powerful storms that hit the U.S. Virgin Islands less than 2 weeks apart in September 2017, caused extensive damage to the natural resources on St. John. Damage was particularly severe in a unique mangrove/coral ecosystem in three bays within Virgin Islands Coral Reef National Monument, a National Park Service marine protected area. Many Red Mangrove (Rhizophora mangle) trees were uprooted and tossed into the sea, and the prop roots of others were stripped of corals, sponges and other marine life. No other mangrove area in the Caribbean is known to have so many scleractinian corals (about 30 species before the storms). Although many corals were overturned or buried in rubble, colonies of most of the species, including four that are listed as threatened under the U.S. Endangered Species Act, survived. Recovery of this ecosystem will depend on Red Mangrove propagules becoming established and producing prop roots to support rich marine life along with a canopy to provide the shade that was critical to the biodiversity that was present before the storms. Unlike in many situations where major disturbances reduce coral cover, the substrate that must be restored for full recovery to occur is a living substrate—the prop roots of the mangroves. Larvae of corals and sponges will need to recruit on to the roots. Future storms could hinder this process.

Effects of sediment resuspension on the larval stage of the model sponge Carteriospongia foliascens

Sponges are important components of many marine communities and perform key functional roles. Little is known on the processes that drive larval dispersal and habitat selection in sponges, and in particular under stress scenarios. The increase in sediment in the marine environment is a growing concern for the health of ecosystems, but scarce information exists on the effects of sediment on sponge larvae. This study assessed the effects of suspended and deposited sediment on the larva of Carteriospongia foliascens. A suspended sediment concentration (SSC) of 100 mg L−1 caused homogenisation of the natural pattern of phototactic responses, leading to 100% of photonegative behaviours and a reduction of swim speeds by 27%. After 24 h exposure to suspended sediments, fine particles were found attached to larval cilia, causing abnormal swimming behaviours. Larvae did not have the ability to remove the attached sediment that led to a transformation of the larval body into a cocoon-like morphology and death. Mortality tripled from 3 mg L−1 (9%) to 300 mg L−1 (30%) and the relative SSC EC10 and EC50 values corresponded to 2.6 mg L−1 and 17.6 mg L−1 respectively. Survival, as determined by live swimming larvae, exceeded 50% even in the highest SSC of 300 mg L−1, however settlement success decreased by ~20%. Larvae were able to settle onto substrate having deposited sediment levels (DSLs) up to 3 mg cm−2 (~24%), but recorded a 25 × chance of dislodgement compared to settlers on substrate with DSL of 0.3 mg cm−2. Larvae avoided settling onto substrates with DSLs >10 mg cm−2 and preferentially settled onto alternative vertical substrate that were free of sediment. While C. foliascens larvae have some ability to survive and settle through conditions of elevated sediment, detrimental effects are also clear.

Sponge Behavior and the Chemical Basis of Responses: A Post-Genomic View.

Sponges perceive and respond to a range of stimuli. How they do this is still difficult to pin down despite now having transcriptomes and genomes of an array of species. Here we evaluate the current understanding of sponge behavior and present new observations on sponge activity in situ. We also explore biosynthesis pathways available to sponges from data in genomes/transcriptomes of sponges and other non-bilaterians with a focus on exploring the role of chemical signaling pathways mediating sponge behavior and how such chemical signal pathways may have evolved. Sponge larvae respond to light but opsins are not used, nor is there a common photoreceptor molecule or mechanism used across sponge groups. Other cues are gravity and chemicals. In situ recordings of behavior show that both shallow and deep-water sponges move a lot over minutes and hours, and correlation of behavior with temperature, pressure, oxygen, and water movement suggests that at least one sponge responds to changes in atmospheric pressure. The sensors for these cues as far as we know are individual cells and, except in the case of electrical signaling in Hexactinellida, these most likely act as independent effectors, generating a whole-body reaction by the global reach of the stimulus to all parts of the animal. We found no evidence for use of conventional neurotransmitters such as serotonin and dopamine. Intriguingly, some chemicals synthesized by symbiont microbes could mean other more complex signaling occurs, but how that interplay might happen is not understood. Our review suggests chemical signaling pathways found in sponges do not reflect loss of a more complex set.

From traveler to homebody: Which signaling mechanisms sponge larvae use to become adult sponges?

Cell-to-cell signaling is responsible for regulation of many developmental processes such as proliferation, cell migration, survival, cell fate specification and axis patterning. In this article we discussed the role of signaling in the metamorphosis of sponges with a focus on epithelial-mesenchymal transition (EMT) accompanying this event. Sponges (Porifera) are an ancient lineage of morphologically simple animals occupying a basal position on the tree of life. The study of these animals is necessary for understanding the origin of multicellularity and the evolution of developmental processes. Development of sponges is quite diverse. It finishes with the metamorphosis of a free-swimming larva into a young settled sponge. The outer surface of sponge larvae consists of a ciliated epithelial sheath, which ensures locomotion, while their internal structure varies from genus to genus. The fate of larval ciliated cells is the most intriguing aspect of metamorphosis. In this review we discuss the fate of larval ciliated cells, the processes going on in cells during metamorphosis at the molecular level and the regulation of this process. The review is based on information about several sponge species with a focus on Halisarca dujardini, Sycon ciliatum and Amphimedon queenslandica. In our model sponge, H. dujardini, ciliated cells leave the larval epithelium during metamorphosis and migrate to the internal cell mass as amoeboid cells to be differentiated into choanocytes of the juvenile sponge. Ciliated cells undergo EMT and internalize within minutes. As EMT involves the disappearance of adherens junctions and as cadherin, the main adherens junction protein, was identified in the transcriptome of several sponges, we suppose that EMT is regulated through cadherin-containing adherens junctions between ciliated cells. We failed to identify the master genes of EMT in the H. dujardini transcriptome, possibly because transcription was absent in the sequenced stages. They may be revealed by a search in the genome. The master genes themselves are controlled by various signaling pathways. Sponges have all the six signaling pathways conserved in Metazoa: Wnt, TGF-beta, Hedgehog, Notch, FGF and NO-dependent pathways. Summarizing the new data about intercellular communication in sponges, we can put forward two main questions regarding metamorphosis: (1) Which of the signaling pathways and in what hierarchical order are involved in metamorphosis? (2) How is the organization of a young sponge related to that of the larva or, in other words, is there a heredity of axes between the larva and the adult sponge?