Adult Sponges Research Articles

The role of photobehaviour in sponge larval dispersal and settlement.

Deciphering the behavioural ecology of adult (sessile) sponges is challenging. However, their motile larval stages afford opportunities to investigate how behaviour contributes to dispersal and selection of habitat. Light is a fundamental cue contributing to larval sponge dispersal where photoreceptive cells contribute to this process. But how universal is light as a cue to sponge larval dispersal and settlement? Behavioural choice experiments were used to test the effect of light on dispersal and settlement behaviours. Larvae of the tropical sponge species Coscinoderma mathewsi, Luffariella variabilis, Ircinia microconnulosa, and Haliclona sp., from deep (12-15 m) and shallower-water habitats (2-5 m), were used in experiments. Dispersal experiments provided a light-gradient-choice where light represented light attenuation with depth. Light treatments included white light and the spectral components of red and blue light. Settlement experiments comprised a choice between illuminated and shaded treatments. Fluorescence microscopy was used to establish the presence of fluorescent proteins associated with posterior locomotory cilia. Deeper-water species, C. mathewsi and I. microconnulosa discriminate light spectral signatures. Both species changed dispersal behaviour to light spectra as larvae aged. For C. mathewsi positive phototaxis to blue light changed to photophobic responses (all light treatments) after six hours and behaviours in I. microconnulosa changed from positive to negative phototaxis (white light) after six hours. L. variabilis, also a deeper-water species, was negatively phototactic to all light treatments. Larvae from the shallow-water species, Haliclona sp., moved towards all light wavelengths tested. There was no effect of light on settlement of the shallow-water Haliclona sp., but larvae in all three deeper-water species showed significantly higher settlement in shaded treatments. Fluorescence microscopy showed discrete fluorescent bands contiguous to posterior tufted cilia in all four species. These fluorescent bands may play a contributory role in larval photobehaviour.

Algal symbionts of the freshwater sponge Ephydatia muelleri

The freshwater sponge, Ephydatia muelleri, is an emerging model system for studying animal:microbe symbioses. Intracellular green microalgae are one of the more common symbionts that live in a facultative mutualism with E. muelleri. While these symbioses have long been known, the identity of the algal symbionts in E. muelleri cells has not been studied in detail. Here, we isolate and characterize endosymbiotic algae from E. muelleri collected from different geographic locations. We find that the algae can be transmitted through asexually produced gemmules and importantly that they can form symbioses with different, differentiated sponge cell types in the adult sponge. Our findings indicate that at least two algal lineages form endosymbioses with E. muelleri. One of the lineages includes species commonly found in samples from two locations in Canada and one in the United States (clade 1: closely related to Auxenochlorella pyrenoidosa). The other clade includes algae found in sponges from one site in Maine, USA, and Lewiniosphaera symbiontica, which is a strain isolated in 1956 from the freshwater sponge Spongilla. We compared microbiomes found in cultures of microalgae as well as the original sponge hosts, and found that very similar bacterial microbiomes associate with both clades (91 orders of Bacteria are shared among the samples we compared). The microbiomes found in the cultures resemble, with a high degree of overlap, the microbiome associated with the sponge host.

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.

Crambe insularis sp. nov. (Crambeidae: Poecilosclerida) a New Crambeid from the Eastern Tropical North Pacific: Morphological, Molecular and Ontogenetic Approach

Specimens of Poecilosclerida taxa, collected from an insular coral community on the Pacific coast of Mexico, were identified as members of the family Crambeidae Lévi, 1963. They were associated with larvae and rhagon phases by using morphological characters, the nucleotide relationship and genetic divergence of three independent loci, two mitochondrial (COI and 16S rDNA) and one ribosomal (28S rDNA C3–C5). Crambe insularis sp. nov. differs from the general skeletal architecture in the genus Crambe Vosmaer, 1880, by its reduced spiculation defined by the presence of ectosomal and choanosomal monactinal megascleres, and the absence of microscleres. Bayesian and Maximum–Likelihood analyses of three loci supported the clustering of larvae, rhagon and adult sponge, all closely related to Mediterranean Crambe crambe (type species of the genus Crambe), and with South American Crambe species (C. chilensis, C. maldonadoi and C. amarilla) as sister species. The larva of C. insularis sp. nov. corresponded to the typical parenchymella larvae poecilosclerid species but with the presence of subtylostyles and styles. Ontogenetic process about the larval and rhagon of this new crambeid are provided. The morphological characters and molecular affinities of Crambe insularis sp. nov. are similar to Monanchora genus, and the implications are further discussed. This is the first taxonomic and molecular study with an integrative approach that includes other diagnostic features such as larval and rhagon development for the description of new species in Porifera.

Global patterns in symbiont selection and transmission strategies in sponges

Sponges host dense and diverse communities of microbes (known as the microbiome) beneficial for the host nutrition and defense. Symbionts in turn receive shelter and metabolites from the sponge host, making their relationship beneficial for both partners. Given that sponge-microbes associations are fundamental for the survival of both, especially the sponge, such relationship is maintained through their life and even passed on to the future generations. In many organisms, the microbiome has profound effects on the development of the host, but the influence of the microbiome on the reproductive and developmental pathways of the sponges are less understood. In sponges, microbes are passed on to oocytes, sperm, embryos, and larvae (known as vertical transmission), using a variety of methods that include direct uptake from the mesohyl through phagocytosis by oocytes to indirect transmission to the oocyte by nurse cells. Such microbes can remain in the reproductive elements untouched, for transfer to offspring, or can be digested to make the yolky nutrient reserves of oocytes and larvae. When and how those decisions are made are fundamentally unanswered questions in sponge reproduction. Here we review the diversity of vertical transmission modes existent in the entire phylum Porifera through detailed imaging using electron microscopy, available metabarcoding data from reproductive elements, and macroevolutionary patterns associated to phylogenetic constraints. Additionally, we examine the fidelity of this vertical transmission and possible reasons for the observed variability in some developmental stages. Our current understanding in marine sponges, however, is that the adult microbial community is established by a combination of both vertical and horizontal (acquisition from the surrounding environment in each new generation) transmission processes, although the extent in which each mode shapes the adult microbiome still remains to be determined. We also assessed the fundamental role of filtration, the cellular structures for acquiring external microbes, and the role of the host immune system, that ultimately shapes the stable communities of prokaryotes observed in adult sponges.

How can environmental variables affect the sexual reproduction of a tropical symbiotic sponge?

In the tropics, the marine sponge Dysidea janiae lives in obligatory symbiosis with the red macroalga Jania adhaerens. However, how this symbiosis is achieved, and how it influences the reproduction of the sponge is still unknown. We analysed the influence of environmental variables on the gametogenesis and embryogenesis of the sponge. We also investigated the histology of the reproductive propagules of the sponge over 3 years, aiming to understand how this symbiosis is established. Dysidea janiae is viviparous and gonochoristic, with a continuous but small reproductive effort. The reproductive dynamics of gametes and embryos were explained by different sets of environmental variables. Although the temperature was not directly related to the reproduction of the sponge in general, there was an increase in the density of spermatic cysts during the year when the El Nino occurred. The day length was related to the embryo dynamics, which were interpreted as an indirect effect of the increase in photosynthetic rates of the symbiont on the energetic budget of the sponge. As no algal propagules were found associated with the eggs or larvae of the sponge, the acquisition of the algae by the sponge is probably a ‘trial-and-error’ relationship after larval release. We propose that the symbiosis increases the fitness of the adult sponge, forcing the larvae to seek new macroalgae to settle on and start a new symbiosis all over again.

Colonización a largo plazo de corales por una esponja excavadora del Caribe

Las ramas muertas de Acropora palmata colonizadas por la esponja excavadora Cliona tenuis son propensas al desplazamiento, la rotura y la translocación durante fuerte oleaje o mar de fondo de tormentas o huracanes, lo que favorece la dispersión de esta esponja. En las islas del Rosario (Colombia, Caribe), los adultos de C. tenuis transportados por fragmentos de A. palmata que cayeron sobre corales masivos vivos colonizaron el nuevo coral y mataron posteriormente el tejido vivo del coral recién invadido. Los corales que reclutaron sobre las ramas caídas de A. palmata cubiertas de C. tenuis también fueron invadidos una vez que la esponja llegó a su base. Para determinar si la incidencia de este fenómeno aumentó desde 2002, cuando se documentó por primera vez, la prevalencia y el modo de colonización de corales por C. tenuis se cuantificó nuevamente en 2014, en el mismo arrecife. Aunque es difícil inferir una tendencia a partir de dos muestreos puntuales, el número de colonias de coral colonizadas por C. tenuis se duplicó en 2014 y se encontraron nuevos casos de colonización desde ramas de A. palmata portadoras de esponjas. Sin embargo, la frecuencia de colonización por esponjas adultas desde las ramas de A. palmata en 2014 fue entre la mitad y un quinto menor que en 2002, lo que sugiere que otras formas de colonización en corales masivos pueden estar aumentando o que las tormentas borran la evidencia de adultos colonizadores por la translocación de las ramas de coral que han servido de vectores, como se observó en un caso monitoreado. A medida que pasa el tiempo y aumenta la fragmentación y la erosión del arrecife, la evidencia de colonización de corales pétreos por C. tenuis a través de las ramas de A. palmata se desvanece.

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.

Regeneration in the sponge Sycon ciliatum partly mimics postlarval development.

Somatic cells dissociated from an adult sponge can reorganize and develop into a juvenile-like sponge, a remarkable phenomenon of regeneration. However, the extent to which regeneration recapitulates embryonic developmental pathways has remained enigmatic. We have standardized and established a sponge Sycon ciliatum regeneration protocol from dissociated cells. Morphological analysis demonstrated that dissociated sponge cells follow a series of morphological events resembling postembryonic development. We performed high-throughput sequencing on regenerating samples and compared the data with that from regular postlarval development. Our comparative transcriptomic analysis revealed that sponge regeneration is as equally dynamic as embryogenesis. We found that sponge regeneration is orchestrated by recruiting pathways similar to those utilized in embryonic development. We also demonstrated that sponge regeneration is accompanied by cell death at early stages, revealing the importance of apoptosis in remodelling the primmorphs to initiate re-development. Because sponges are likely to be the first branch of extant multicellular animals, we suggest that this system can be explored to study the genetic features underlying the evolution of multicellularity and regeneration.

In Search of the Ancestral Organization and Phylotypic Stage of Porifera

Each animal phylum has its own bauplan. The phylotypic stage is the ontogenetic stage during which the phylum level characteristics appear. This stage refers to different stages of development in different animals. Sponges are one of the simplest, and probably the oldest multicellular lineage of extant animals. On the basis of the analysis of sponge development during (i) sexual and asexual reproduction, (ii) regeneration from small body fragments, and (iii) cell reaggregation, we suggest a hypothetical variant of their phylotypic stage (spongotype): the mono-oscular juvenile—the rhagon. The major feature, which permits to consider the rhagon as the phylotypic stage of the Porifera is the final, definitive position of all the cellular and anatomical elements of the future adult sponge. It seems that at the rhagon stage the pattern of the axial complex of anlagen is already formed, and only growth processes occur at the later stages.

Kinetid structure in larval and adult stages of the demosponges Haliclona aquaeductus (Haplosclerida) and Halichondria panicea (Suberitida)

At larval and adult stage of life cycle, sponges (Porifera) have different flagellated cells that play different roles in their body. The larval epithelium cells serve as locomotion organs, while adult collar cells (choanocytes) have a feeding function. Here, for the first time, we describe detailed structure of the flagellar apparatus (kinetid) in larval cells and choanocytes of Haliclona aquaeductus and Halichondria panicea demosponges, and attach schemes of its organization, based on longitudinal and transversal ultrathin serial sections. The kinetid of larvae has proved to be more complicated than the choanocytes ones. It includes well-developed transverse and longitudinal cytoskeletons that strengthen the larval flagellum. The longitudinal skeleton in H. aquaeductus is represented by unusual structures, which were previously understudied: large tubular rootlets made of oblique-crossed fibers, which connect the kinetosome with mitochondria. We also found out that the kinetid composition varies between different cell types of a highly structured parenchymella of H. aquaeductus. In simply organized parenchymella of H. panicea, flagellated cells are identical and its kinetid includes a permanent additional centriole absent in choanocytes of adult sponges. We tried to evaluate the diversity of sponge larval kinetid organization based on literature data and found it variable within Haplosclerida and quite conservative within other sponge lineages.

The Precursor Hypothesis of Sponge Kleptocnidism: Development of Nematocysts in Haliclona cnidata sp. nov. (Porifera, Demospongiae, Haplosclerida)

Marine sponges thrive in benthic environments despite intense spatial competition and predator pressure. The sessile filter feeders usually compensate their lack of physical defense and behavioral escape by a high level of bioactivity. In the stinging black sponge (Haliclona cnidata sp. nov.), these chemical defense mechanisms are complemented by ‘cellular weapons’ – functional nematocysts likely acquired from cnidarians (kleptocnidism). Whereas kleptocnidism might be facilitated by a close contact with cnidarian donors, preliminary investigations suggest that the stinging black sponge sustains nematocysts even if kept apart from cnidarians. As the underlying mechanisms causing this phenomenon remain unknown, the development of its nematocysts was studied in both presence and absence of potential cnidarian donors. First, we compared inherent nematocysts of adult sponge individuals with foreign nematocysts of co-cultivated cnidarians to identify potential donors. Second, we experimentally assessed the donor independent and donor dependent development of inherent and foreign nematocysts within cultures of sponge cell aggregates (SCAs). The inherent nematocysts comprised two specific types that both differed from those of the eight co-cultivated cnidarians. Specifically, we showed that the number of sponge-inherent nematocysts increased in SCAs over time in the absence of potential donors. Numbers of supplied foreign nematocysts, however, did not increase in the SCAs. We conclude that the observed increase of inherent kleptocnidae nematocysts is due to the maturation of nematocyst precursor cells. Given these findings, we here propose the precursor hypothesis of sponge kleptocnidism. Accordingly, nematocyst precursors or immature nematocyte-nematocyst complexes might be initially acquired by sponges through filtration, maintained in sponge tissues, and nurtured to fully functioning nematocyte-nematocyst complexes. The underlying evolutionary processes are likely facilitated by bacteria derived secondary metabolites and photosynthetically active dinoflagellates. Due to a simple body plan and the in vitro proliferation capacity of sponge cells, Haliclona cnidata sp. nov. may serve as a novel evolutionary model system to further assess fundamental research questions regarding kleptocnidism. This study not only sheds new light on kleptocnidism in sponges, it also calls for a holobiontic view at defense mechanisms that involves the actual sponge, cnidarian nematocysts, dinoflagellate endosymbionts, and a complex microbial community.

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?

Effects of combined dredging-related stressors on sponges: a laboratory approach using realistic scenarios

Dredging can cause increased suspended sediment concentrations (SSCs), light attenuation and sedimentation in marine communities. In order to determine the combined effects of dredging-related pressures on adult sponges, three species spanning different nutritional modes and morphologies were exposed to 5 treatment levels representing realistic dredging scenarios. Most sponges survived under low to moderate turbidity scenarios (SSCs of ≤ 33 mg L−1, and a daily light integral of ≥0.5 mol photons m−2 d−1) for up to 28 d. However, under the highest turbidity scenario (76 mg L−1, 0.1 mol photons m−2 d−1) there was 20% and 90% mortality of the phototrophic sponges Cliona orientalis and Carteriospongia foliascens respectively, and tissue regression in the heterotrophic Ianthella basta. All three sponge species exhibited mechanisms to effectively tolerate dredging-related pressures in the short term (e.g. oscula closure, mucus production and tissue regression), although reduced lipids and deterioration of sponge health suggest that longer term exposure to similar conditions is likely to result in higher mortality. These results suggest that the combination of high SSCs and low light availability can accelerate mortality, increasing the probability of biological effects, although there is considerable interspecies variability in how adult sponges respond to dredging pressures.

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

Vertical transmission of bacterial symbionts, which is known in many species of sponge (Porifera), is expected to promote strong fidelity between the partners. Combining 16S rRNA gene amplicon sequencing and electron microscopy, we have assayed the relative abundance of vertically-inherited bacterial symbionts in several stages of the life cycle of Amphimedon queenslandica, a tropical coral reef sponge. We reveal that adult A. queenslandica house a low diversity microbiome dominated by just three proteobacterial OTUs, with a single gammaprotebacterium clearly dominant through much of the life cycle. This ontogenetic perspective has revealed that, although vertical transmission occurs very early in development, the inherited symbionts do not maintain proportional dominance of the bacterial community at every developmental stage. A reproductive bottleneck in the A. queenslandica life cycle is larval settlement, when a free-swimming pelagic larva settles out of the water column onto the benthos and completes metamorphoses into the sessile body plan within just 3 to 4 days. During this dramatic life cycle transition, an influx of environmentally-derived bacteria leads to a major reorganization of the microbiome, potentially challenging the fidelity and persistence of the vertically-inherited symbiotic relationships. However, dominance of the primary, vertically-inherited symbionts is restored in adult sponges. The mechanisms underlying ontogenetic changes in the bacterial community are unknown, including how the dominance of the primary symbionts is restored in the adult sponge – does the host or symbiont regulate this process? Using high-resolution transcriptional profiling in multiple stages of the A. queenslandica life cycle combined with this natural perturbation of the microbiome immediately following larval settlement, we are beginning to identify candidate host genes associated with animal-bacterial crosstalk. Among the sponge host genes upregulated during the times of active microbiome assembly, there is an enrichment of genes potentially involved in innate immunity, including scavenger receptors, and of genes containing eukaryote-like domains, which have elsewhere been implicated in host-symbiont interactions. Intriguingly, we also see an enrichment of sponge genes arising from ancient horizontal transfer events from bacteria, which raises the possibility that host-bacterial associations in the evolutionary past may help to regulate host-bacterial associations in the ecological present.

Interactive effects of temperature and pCO2 on sponges: from the cradle to the grave.

As atmospheric CO2 concentrations rise, associated ocean warming (OW) and ocean acidification (OA) are predicted to cause declines in reef-building corals globally, shifting reefs from coral-dominated systems to those dominated by less sensitive species. Sponges are important structural and functional components of coral reef ecosystems, but despite increasing field-based evidence that sponges may be 'winners' in response to environmental degradation, our understanding of how they respond to the combined effects of OW and OA is limited. To determine the tolerance of adult sponges to climate change, four abundant Great Barrier Reef species were experimentally exposed to OW and OA levels predicted for 2100, under two CO2 Representative Concentration Pathways (RCPs). The impact of OW and OA on early life-history stages was also assessed for one of these species to provide a more holistic view of species impacts. All species were generally unaffected by conditions predicted under RCP6.0, although environmental conditions projected under RCP8.5 caused significant adverse effects: with elevated temperature decreasing the survival of all species, increasing levels of tissue necrosis and bleaching, elevating respiration rates and decreasing photosynthetic rates. OA alone had little adverse effect, even under RCP8.5 concentrations. Importantly, the interactive effect of OW and OA varied between species with different nutritional modes, with elevated pCO2 exacerbating temperature stress in heterotrophic species but mitigating temperature stress in phototrophic species. This antagonistic interaction was reflected by reduced mortality, necrosis and bleaching of phototrophic species in the highest OW/OA treatment. Survival and settlement success of Carteriospongia foliascens larvae were unaffected by experimental treatments, and juvenile sponges exhibited greater tolerance to OW than their adult counterparts. With elevated pCO2 providing phototrophic species with protection from elevated temperature, across different life stages, climate change may ultimately drive a shift in the composition of sponge assemblages towards a dominance of phototrophic species.

Field and laboratory investigations of budding in the tetillid sponge Cinachyrella cavernosa

AbstractThe budding process of the tetillid sponge Cinachyrella cavernosa was studied for one year in the low intertidal zone near Mhapan (15°55′27.48″N, 73°33′29.89″E), on the central west coast of India. The sponges showed the highest budding frequency when the average water temperature of intertidal rock pools was 32.4±0.23°C (February–March), followed by a significant decrease in budding frequency at 28.2±0.12°C (April–July), and no budding at ≤25.9±0.12°C (August–November). Stepwise multiple regression analysis of physico‐chemical factors revealed temperature as the most prominent factor regulating the intensity of budding. Based on size and morphology, three stages of sponge buds were defined. The production of buds was found to be asynchronous, as adult sponges possessed buds of all three stages. Differences among these stages were examined at ultrastructural (in terms of spicules) and molecular (in terms of RNA/DNA) levels. Stage I (<0.5 mm dia‐meter) buds showed a complete absence of microscleres (sigmaspires), whereas stage II (0.5–1 mm) and stage III (>1 mm) buds contained all spicules characteristic of the adult sponge. There was a significant increase in RNA/DNA ratio from stage I to III, suggestive of a progressive increase in physiological activity during the developmental process. Additionally, we studied post‐settlement bud growth under field and laboratory conditions. Newly settled buds displayed a lower average‐specific growth rate in the field, owing to variability in environmental conditions, but more rapid growth under controlled conditions in the laboratory. This study highlights the role of abiotic factors in regulating the budding process and stresses the ecological significance of budding in maintaining natural sponge populations. Our data suggest that an increased frequency of budding under stressful conditions, such as high temperature, is an advantageous adaptation for these sponges. Buds showed rapid development, as no metamorphosis is involved, and retained the genotype of the parents, yielding high reproductive outputs and survival rates.

Environmental heterogeneity and microbial inheritance influence sponge-associated bacterial composition of Spongia lamella.

Sponges are important components of marine benthic communities. High microbial abundance sponges host a large diversity of associated microbial assemblages. However, the dynamics of such assemblages are still poorly known. In this study, we investigated whether bacterial assemblages present in Spongia lamella remained constant or changed as a function of the environment and life cycle. Sponges were collected in multiple locations and at different times of the year in the western Mediterranean Sea and in nearby Atlantic Ocean to cover heterogeneous environmental variability. Co-occurring adult sponges and offsprings were compared at two of the sites. To explore the composition and abundance of the main bacteria present in the sponge mesohyl, embryos, and larvae, we applied both 16S rRNA gene-denaturing gradient gel electrophoresis (DGGE) and sequencing of excised DGGE bands and quantitative polymerase chain reactions (qPCR). On average, the overall core bacterial assemblage showed over 60 % similarity. The associated bacterial assemblage fingerprints varied both within and between sponge populations, and the abundance of specific bacterial taxa assessed by qPCR significantly differed among sponge populations and between adult sponge and offsprings (higher proportions of Actinobacteria in the latter). Sequences showed between 92 and 100 % identity to sequences previously reported in GenBank, and all were affiliated with uncultured invertebrate bacterial symbionts (mainly sponges). Sequences were mainly related to Chloroflexi and Acidobacteria and a few to Actinobacteria and Bacteroidetes. Additional populations may have been present under detection limits. Overall, these results support that both ecological and biological sponge features may shape the composition of endobiont bacterial communities in S. lamella.

A complex life cycle in a warming planet: gene expression in thermally stressed sponges

Sponges are abundant, diverse and functionally important components of aquatic biotopes with crucial associations for many reef fish and invertebrates. Sponges have strict temperature optima, and mass mortality events have occurred after unusually high temperatures. To assess how sponges may adapt to thermal stress associated with a changing climate, we applied gene expression profiling to both stages of their bipartite life cycles. Adult Rhopaloeides odorabile are highly sensitive to thermal stress (32 °C), yet their larvae can withstand temperatures up to 36 °C. Here, we reveal the molecular mechanisms that underpin these contrasting thermal tolerances, which may provide sponges with a means to successfully disperse into cooler waters. Heat shock protein 70 was induced by increasing temperature in adult sponges, and genes involved in important biological functions including cytoskeleton rearrangement, signal transduction, protein synthesis/degradation, oxidative stress and detoxification were all negatively correlated with temperature. Conversely, gene expression in larvae was not significantly affected until 36 °C when a stress response involving extremely rapid activation of heat shock proteins occurred. This study provides the first transcriptomic assessment of thermal stress on both life history stages of a marine invertebrate facilitating better predictions of the long-term consequences of climate change for sponge population dynamics.

Ectyoplasia ferox, an Experimentally Tractable Model for Vertical Microbial Transmission in Marine Sponges

The oviparous sponge Ectyoplasia ferox is commonly found in Florida and the Bahamas. Every year in August and/or September about 6 days after a full moon, E. ferox will shed embryo-containing spawning material into the seawater from which hundreds to thousands of larvae will hatch per host individual. In order to investigate vertical microbial transmission in E. ferox, 16S rRNA gene library construction and denaturing gradient gel electrophoresis was employed. Microbial symbionts from six phyla and the unknown lineage SAUL were shown to be vertically transmitted. The identification of 21 VT clusters, of which 19 were situated within sponge-specific or sponge-coral-specific clusters, indicated that a large fraction of the symbiotic microbial consortium was present in the sexual reproductive stages. Spawning led to a 50 % reduction of microbial numbers in the adult sponge mesohyl. We furthermore provide the first evidence that the symbiotic microbial consortia of E. ferox were generally metabolically active within the reproductive stages. Finally, we propose E. ferox as a model system for vertical transmission owing to the ease of experimental access to all sexual reproductive stages, and to experimental tractability in the laboratory including the possibility of rearing symbiont-free juvenile sponges.