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Coral reefs in the northern Red Sea experience strong seasonality. This affects reef carbon (C) cycling, but ecosystem-wide quantification of C fluxes in such reefs is limited. This study quantified seasonal reef community C fluxes with incubations. Resulting data were then incorporated into seasonal linear inverse models (LIM). For spring, additional sponge incubation results allowed for unique assessment of the contribution of sponges to C cycling. The coral reef ecosystem was heterotrophic throughout all seasons as gross community primary production (GPP; 136–200, range of seasonal means in mmol C m−2 d−1) was less than community respiration (R; 192–279), and balanced by import of organic carbon (52–100), 88‒92% of which being dissolved organic carbon (DOC). Hard coral GPP (74–110) and R (100–137), as well as pelagic bacteria DOC uptake (58–101) and R (42–86), were the largest C fluxes across seasons. The ecosystem was least heterotrophic in spring (highest irradiance) (GPP:R 0.81), but most heterotrophic in summer and fall with higher water temperatures (0.68 and 0.60, respectively). Adding the sponge community to the model increased community R (247 ± 8 without to 353 ± 13 with sponges (mean ± SD)). Sponges balanced this demand primarily with DOC uptake (105 ± 6, 97% by cryptic sponges). This rate is comparable to the uptake of DOC by pelagic bacteria (104 ± 5) placing the cryptic sponges among the dominant C cycling groups in the reef.

In this study, we used 16S rRNA gene amplicon sequencing to investigate prokaryotic community composition of the Caribbean sponges Xestospongia muta and Agelas sventres from three depth ranges: X. muta was enriched in Cyanobacteria, Chloroflexota, and Crenarchaeota compared to samples from mesophotic depths, while mesophotic samples of X. muta were enriched in Acidobacteriota. For A. sventres, relative abundance of Acidobacteriota, Chloroflexota, and Gammaproteobacteria was higher in shallow samples, while Proteobacteria and Crenarchaeota were enriched in mesophotic A. sventres samples. Antimicrobial activity was evaluated by screening crude extracts of sponges against a set of Gram-positive and Gram-negative bacteria, a yeast, and an oomycete. Antibacterial activities from crude extracts of shallow sponge individuals were generally higher than observed from mesophotic individuals, that showed limited or no antibacterial activities. Conversely, the highest anti-oomycete activity was found from crude extracts of X. muta individuals from lower mesophotic depth, but without a clear pattern across the depth gradient. These results indicate that sponge-associated prokaryotic communities and the antimicrobial activity of sponges change within species across a depth gradient from shallow to mesophotic depth.

Sponges, among the oldest extant multicellular organisms on Earth,1 play a key role in the cycling of nutrients in many aquatic ecosystems.2-5 They need to employ strategies to prevent clogging of their internal filter system by solid wastes,6-8 but self-cleaning mechanisms are largely unknown. It is commonly assumed that sponges remove solid waste with the outflowing water through distinct outflow openings (oscula).3,9 Here, we present time-lapse video footage and analyses of sponge waste revealing a completely different mechanism of particle removal in the Caribbean tube sponge Aplysina archeri. This sponge actively moves particle-trapping mucus against the direction of its internal water flow and ejects it into the surrounding water from its seawater inlet pores (ostia) through periodic surface contractions that have been described earlier as "sneezing."10,11 Visually, it appears as if the sponge is continuously streaming mucus-embedded particles and sneezes to shed this particulate waste, resulting in a notable flux of detritus that is actively consumed by sponge-associated fauna. The new data are used to estimate production of detritus for this abundant sponge on Caribbean coral reefs. Last, we discuss why waste removal from the sponge inhalant pores may be a common feature among sponges and compare the process in sponges to equivalent mechanisms of mucus transport in other animals, including humans.

The ability of organisms to combine autotrophy and heterotrophy gives rise to one of the most successful nutritional strategies on Earth: mixotrophy. Sponges are integral members of shallow-water ecosystems and many host photosynthetic symbionts, but studies on mixotrophic sponges have focused primarily on species residing in high-light environments. Here, we quantify the contribution of photoautotrophy to the respiratory demand and total carbon diet of the sponge Chondrilla caribensis, which hosts symbiotic cyanobacteria and lives in low-light environments. Although the sponge is net heterotrophic at 20 m water depth, photosynthetically fixed carbon potentially provides up to 52% of the holobiont’s respiratory demand. When considering the total mixotrophic diet, photoautotrophy contributed an estimated 7% to total daily carbon uptake. Visualization of inorganic 13C- and 15N-incorporation using nanoscale secondary ion mass spectrometry (NanoSIMS) at the single-cell level confirmed that a portion of nutrients assimilated by the prokaryotic community was translocated to host cells. Photoautotrophy can thus provide an important supplemental source of carbon for sponges, even in low-light habitats. This trophic plasticity may represent a widespread strategy for net heterotrophic sponges hosting photosymbionts, enabling the host to buffer against periods of nutritional stress.

A paramount challenge in coral reef ecology is to estimate the abundance and composition of the communities residing in such complex ecosystems. Traditional 2D projected surface cover estimates neglect the 3D structure of reefs and reef organisms, overlook communities residing in cryptic reef habitats (e.g., overhangs, cavities), and thus may fail to represent biomass estimates needed to assess trophic ecology and reef function. Here, we surveyed the 3D surface cover, biovolume, and biomass (i.e., ash-free dry weight) of all major benthic taxa on 12 coral reef stations on the island of Curaçao (Southern Caribbean) using structure-from-motion photogrammetry, coral point counts, in situ measurements, and elemental analysis. We then compared our 3D benthic community estimates to corresponding estimates of traditional 2D projected surface cover to explore the differences in benthic community composition using different metrics. Overall, 2D cover was dominated (52 ± 2%, mean ± SE) by non-calcifying phototrophs (macroalgae, turf algae, benthic cyanobacterial mats), but their contribution to total reef biomass was minor (3.2 ± 0.6%). In contrast, coral cover (32 ± 2%) more closely resembled coral biomass (27 ± 6%). The relative contribution of erect organisms, such as gorgonians and massive sponges, to 2D cover was twofold and 11-fold lower, respectively, than their contribution to reef biomass. Cryptic surface area (3.3 ± 0.2 m2 m−2planar reef) comprised half of the total reef substrate, rendering two thirds of coralline algae and almost all encrusting sponges (99.8%) undetected in traditional assessments. Yet, encrusting sponges dominated reef biomass (35 ± 18%). Based on our quantification of exposed and cryptic reef communities using different metrics, we suggest adjustments to current monitoring approaches and highlight ramifications for evaluating the ecological contributions of different taxa to overall reef function. To this end, our metric conversions can complement other benthic assessments to generate non-invasive estimates of the biovolume, biomass, and elemental composition (i.e., standing stocks of organic carbon and nitrogen) of Caribbean coral reef communities. Supplementary Information The online version contains supplementary material available at 10.1007/s00338-021-02118-6.

Sponge-microbe symbioses underpin the ecological success of sponges in many aquatic benthic ecosystems worldwide. These symbioses are often described as mutually beneficial, but identifying positive symbiotic interactions and quantifying the contribution of partners to physiological processes is challenging. For example, our understanding of the relative contribution of sponge cells and their microbial symbionts to the uptake and exchange of dissolved organic matter (DOM)—a major component of sponge diet—is limited. Here, we combined host-symbiont cell separation with pulse-chase isotopic labelling in order to trace the uptake of 13C- and 15Nenriched DOM into sponge cells and microbial symbionts of the encrusting Caribbean sponges Haliclona vansoesti and Scopalina ruetzleri, which are low microbial abundance (LMA) species. Sponge cells were responsible for >99% of DOM assimilation during the pulse-chase experiment for both sponge species, while the contribution of symbiotic microbes to total DOM uptake was negligible (

This mini-review evaluates the use of marine sponges in integrated culture systems, two decades after the idea was first proposed. It was predicted that the concept would provide a double benefit: sponges would grow faster under higher organic loadings, and filtration by sponges would improve water quality. It is promising that the growth of some commercially interesting sponges is indeed faster in organically enriched areas. The applicability of sponges as filters for undesired microorganisms has been confirmed in laboratory studies. However, upscaled farming studies need to be done to demonstrate the value of sponges for in situ bioremediation of sewage discharge or waste produced by fish cages. In addition, a new idea is presented – the use of sponges as an engine to convert dissolved organic matter (DOM) into particulate organic matter (POM) that can be consumed by deposit feeders through a chain of processes termed the sponge loop. A theoretical design of an integrated culture with seaweeds (Gracilaria sp.), sponges (Halisarca caerulea) and sea cucumbers (Apostichopus japonica) shows that 37% of the part of the primary production that is excreted by the seaweeds as DOM can be directly recovered in sponge biomass and a subsequent 12% in sea cucumber biomass after mediation (conversion of DOM to POM) by sponges. Hence, the total recovery of DOM into (sponge and sea cucumber) biomass within this IMTA is 49%.

Marine sponges play a major ecological role in recycling resources on coral reef ecosystems. The cycling of resources may largely depend on the stability of the host–microbiome interactions and their susceptibility to altered environmental conditions. Given the current coral to algal phase shift on coral reefs, we investigated whether the sponge-associated bacterial communities of four sponge species, with either high or low microbial abundances (HMA and LMA), remain stable at two reefs sites with different coral to algae cover ratios. Additionally, we assessed the bacterial community composition of two of these sponge species before and after a reciprocal transplantation experiment between the sites. An overall stable bacterial community composition was maintained across the two sites in all sponge species, with a high degree of host-specificity. Furthermore, the core bacterial communities of the sponges remained stable also after a 21-day transplantation period, although a minor shift was observed in less abundant taxa (< 1%). Our findings support the conclusion that host identity and HMA–LMA status are stronger traits in shaping bacterial community composition than habitat. Nevertheless, long-term microbial monitoring of sponges along with benthic biomass and water quality assessments are needed for identifying ecosystem tolerance ranges and tipping points in ongoing coral reef phase shifts., Analysis of four different sponge holobionts reveals that their associated bacterial communities are host-specific and remain stable across habitats with different coral to algae cover ratios.

The increased release of dissolved organic matter (DOM) by algae has been associated with the fast but inefficient growth of opportunistic microbial pathogens and the ongoing degradation of coral reefs. Turf algae (consortia of microalgae and macroalgae commonly including cyanobacteria) dominate benthic communities on many reefs worldwide. Opposite to other reef algae that predominantly release DOM during the day, turf algae containing cyanobacteria may additionally release large amounts of DOM at night. However, this night-DOM release and its potential contribution to the microbialization of reefs remains to be investigated.We first tested the occurrence of hypoxic conditions at the turf algae-water interface, as a lack of oxygen will facilitate the production and release of fermentation intermediates as night-time DOM. Second, the dissolved organic carbon (DOC) release by turf algae was quantified during day time and nighttime, and the quality of day and night exudates as food for bacterioplankton was tested. Finally, DOC release rates of turf algae were combined with estimates of DOC release based on benthic community composition in 1973 and 2013 to explore how changes in benthic community composition affected the contribution of night-DOC to the reef-wide DOC production.A rapid shift from supersaturated to hypoxic conditions at the turf algae-water interface occurred immediately after the onset of darkness, resulting in night-DOC release rates similar to those during daytime. Bioassays revealed major differences in the quality between day and night exudates: Night-DOC was utilized by bacterioplankton two times faster than day-DOC, but yielded a four times lower growth efficiency. Changes in benthic community composition were estimated to have resulted in a doubling of DOC release since 1973, due to an increasing abundance of benthic cyanobacterial mats (BCMs), with night-DOC release by BCMs and turf algae accounting for50% of the total release over a diurnal cycle.Night-DOC released by BCMs and turf algae is likely an important driver in the microbialization of reefs by stimulating microbial respiration at the expense of energy and nutrient transfer to higher trophic levels via the microbial loop, thereby threatening the productivity and biodiversity of these unique ecosystems. Read the free Plain Language Summary for this article on the Journal blog.El incremento de la liberación de materia orgánica disuelta (MOD) por parte de las algas se ha asociado con el crecimiento rápido pero ineficaz de microorganismos patógenos oportunistas y la continua degradación de los arrecifes coralinos. Los céspedes algales (consorcios de micro y macroalgas que suelen incluir cianobacterias) dominan las comunidades bentónicas de muchos arrecifes de todo el mundo. A diferencia de otras algas de arrecife que liberan predominantemente MOD durante el día, los céspedes algales que contienen cianobacterias pueden liberar adicionalmente grandes cantidades de MOD durante la noche. Sin embargo, esta liberación nocturna de MOD y su potencial contribución a la microbialización de los arrecifes aún falta por ser investigada.En primer lugar, investigamos la existencia de condiciones de hipoxia en la interfase entre los céspedes algales y el agua, ya que la falta de oxígeno facilitaría la producción y liberación de productos intermedios de fermentación como MOD nocturna. En segundo lugar, cuantificamos la liberación de carbono orgánico disuelto (COD) por los céspedes algales durante el día y la noche, y se comprobó la calidad de los exudados diurnos y nocturnos como alimento para el bacterioplancton. Finalmente, las tasas de liberación de MOD de los céspedes algales se combinaron con las estimaciones de liberación de COD basadas en la composición de la comunidad bentónica en 1973 y 2013 para explorar cómo los cambios en la composición de la comunidad bentónica afectaron a la contribución de MOD nocturna y a su vez a la producción de COD en todo el arrecife.En ausencia de luz, se produjo inmediatamente un cambio rápido de condiciones sobresaturadas a condiciones hipóxicas en la interfaz entre los céspedes algales y el agua, lo que dio lugar a tasas de liberación de COD nocturnas similares a las diurnas. Los bioensayos revelaron importantes diferencias en la calidad de los exudados diurnos y nocturnos: el bacterioplancton utilizó el COD nocturno dos veces más rápido que el COD diurno, pero su eficiencia de crecimiento fue cuatro veces menor. Se estimó que los cambios en la composición de la comunidad bentónica han dado lugar a una duplicación de la liberación de MOD desde 1973 debido a la creciente abundancia de tapetes de cianobacterias bentónicas, y que la liberación nocturna de COD por parte de estos tapetes y los céspedes algales representa50% de la liberación total durante un ciclo diurno.El COD nocturno que es liberado por los tapetes de cianobacterias bentónicas y los céspedes algales es probablemente un importante promotor de la microbialización de los arrecifes al estimular la respiración microbiana a expensas de la transferencia de energía y nutrientes a los niveles tróficos superiores a través del bucle microbiano y, por tanto, amenaza la productividad y la biodiversidad de estos ecosistemas únicos.

Cold-water coral reefs and sponge grounds are deep-sea biological hotspots, equivalent to shallow-water tropical coral reefs. In tropical ecosystems, biodiversity and productivity are maintained through efficient recycling pathways, such as the sponge loop. In this pathway, encrusting sponges recycle dissolved organic matter (DOM) into particulate detritus. Subsequently, the sponge-produced detritus serves as a food source for other organisms on the reef. Alternatively, the DOM stored in massive sponges was recently hypothesized to be transferred to higher trophic levels through predation of these sponges, instead of detritus production. However, for deep-sea sponges, the existence of all prerequisite, consecutive steps of the sponge loop have not yet been established. Here, we tested whether cold-water deep-sea sponges, similar to their tropical shallow-water counterparts, take up DOM and transfer assimilated DOM to associated fauna via either detritus production or predation. We traced the fate of 13carbon (C)- and 15nitrogen (N)-enriched DOM and particulate organic matter (POM) in time using a pulse-chase approach. During the 24-h pulse, the uptake of 13C/15N-enriched DOM and POM by two deep-sea sponge species, the massive species Geodia barretti and the encrusting species Hymedesmia sp., was assessed. During the subsequent 9-day chase in label-free seawater, we investigated the transfer of the consumed food by sponges into brittle stars via two possible scenarios: (1) the production and subsequent consumption of detrital waste or (2) direct feeding on sponge tissue. We found that particulate detritus released by both sponge species contained C from the previously consumed tracer DOM and POM, and, after 9-day exposure to the labeled sponges and detritus, enrichment of 13C and 15N was also detected in the tissue of the brittle stars. These results therefore provide the first evidence of all consecutive steps of a sponge loop pathway via deep-sea sponges. We cannot distinguish at present whether the deep-sea sponge loop is acting through a detrital or predatory pathway, but conclude that both scenarios are feasible. We conclude that sponges could play an important role in the recycling of DOM in the many deep-sea ecosystems where they are abundant, although in situ measurements are needed to confirm this hypothesis.

Sponges are ubiquitous components of various deep‐sea habitats, including cold water coral reefs, and form deep‐sea sponge grounds. Although the deep sea is generally considered to be a food‐limited environment, these ecosystems are known to be hotspots of biodiversity and carbon cycling. To assess the role of sponges in the carbon cycling of deep‐sea ecosystems, we studied the carbon budgets of six dominant deep‐sea sponges of different phylogenetic origin, with various growth forms and hosting distinct associated microbial communities, in an ex situ aquarium setup. Additionally, we determined biomass metrics—planar surface area, volume, wet weight, dry weight (DW), ash‐free dry weight, and organic carbon (C) content—and conversion factors for all species. Oxygen (O2) removal rates averaged 3.3 ± 2.8 μmol O2 g DWsponge h−1 (mean ± SD), live particulate (bacterio‐ and phytoplankton) organic carbon removal rates averaged 0.30 ± 0.39 μmol C g DWsponge h−1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 μmol C g DWsponge h−1. Carbon mass balances were calculated for four species and revealed that the sponges acquired 1.3–6.6 times the amount of carbon needed to sustain their minimal respiratory demands. These results indicate that irrespective of taxonomic class, growth form, and abundance of microbial symbionts, DOC is responsible for over 90% of the total net organic carbon removal of deep‐sea sponges and allows them to sustain themselves in otherwise food‐limited environments on the ocean floor.

Sponges produce distinct fatty acids (FAs) that (potentially) can be used as chemotaxonomic and ecological biomarkers to study endosymbiont-host interactions and the functional ecology of sponges. Here, we present FA profiles of five common habitat-building deep-sea sponges (class Demospongiae, order Tetractinellida), which are classified as high microbial abundance (HMA) species. Geodia hentscheli, G. parva, G. atlantica, G. barretti, and Stelletta rhaphidiophora were collected from boreal and Arctic sponge grounds in the North-Atlantic Ocean. Bacterial FAs dominated in all five species and particularly isomeric mixtures of mid-chain branched FAs (MBFAs, 8- and 9-Me-C16:0 and 10 and 11-Me-C18:0) were found in high abundance (together ≥ 20% of total FAs) aside more common bacterial markers. In addition, the sponges produced long-chain linear, mid- and a(i)-branched unsaturated FAs (LCFAs) with a chain length of 24‒28 C atoms and had predominantly the typical Δ5,9 unsaturation, although also Δ9,19 and (yet undescribed) Δ11,21 unsaturations were identified. G. parva and S. rhaphidiophora each produced distinct LCFAs, while G. atlantica, G. barretti, and G. hentscheli produced similar LCFAs, but in different ratios. The different bacterial precursors varied in carbon isotopic composition (δ13C), with MBFAs being more enriched compared to other bacterial (linear and a(i)-branched) FAs. We propose biosynthetic pathways for different LCFAs from their bacterial precursors, that are consistent with small isotopic differences found in LCFAs. Indeed, FA profiles of deep-sea sponges can serve as chemotaxonomic markers and support the conception that sponges acquire building blocks from their endosymbiotic bacteria.

Sponges are ubiquitous components of various deep-sea habitats, including cold water coral reefs and deep-sea sponge grounds. Despite being surrounded by oligotrophic waters, these ecosystems are known to be hotspots of biodiversity and carbon cycling. To assess the role of sponges in the carbon cycling of deep-sea ecosystems, we studied the energy budgets of six dominant deep-sea sponges (the hexactinellid species Vazella pourtalesi, and demosponge species Geodia barretti, Geodia atlantica, Craniella zetlandica, Hymedesmia paupertas and Acantheurypon spinispinosum) in an ex situ aquarium setup. Additionally, we determined morphological metrics for all species (volume, dry weight (DW), wet weight (WW), carbon (C) content, and ash-free dry weight (AFDW)) and provide species-specific conversion factors. Oxygen (O2) removal rates averaged 3.3 ± 2.8 µmol O2 DWsponge h−1 (all values mean ± SD), live particulate (bacterial and phytoplankton) organic carbon (LPOC) removal rates averaged 0.30 ± 0.39 µmol C DWsponge h−1 and dissolved organic carbon (DOC) removal rates averaged 18.70 ± 25.02 µmol C DWsponge h−1. Carbon mass balances were calculated for four species (V. pourtalesi, G. barretti, G. atlantica and H. paupertas) and revealed that the sponges acquired 1.3–6.6 times the amount of carbon needed to sustain their minimal respiratory demands. These results indicate that irrespective of taxonomic class, growth form, and abundance of microbial symbionts, DOC is responsible for over 90 % of the total net organic carbon removal of deep-sea sponges and allows them to sustain in otherwise food-limited environments on the ocean floor.

Background Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of 13C- and 15N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea. Results The two sponge species showed significant enrichment of DOM- and POM-derived 13C and 15N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome. Conclusions Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan–microbe symbioses.

Marine sponges often host diverse and species-specific communities of microorganisms that are critical for host health. Previous functional genomic investigations of the sponge microbiome have focused primarily on specific symbiont lineages, which frequently make up only a small fraction of the overall community. Here, we undertook genome-centric analysis of the symbiont community in the model species Ircinia ramosa and analyzed 259 unique, high-quality metagenome-assembled genomes (MAGs) that comprised 74% of the I. ramosa microbiome. Addition of these MAGs to genome trees containing all publicly available microbial sponge symbionts increased phylogenetic diversity by 32% within the archaea and 41% within the bacteria. Metabolic reconstruction of the MAGs showed extensive redundancy across taxa for pathways involved in carbon fixation, B-vitamin synthesis, taurine metabolism, sulfite oxidation, and most steps of nitrogen metabolism. Through the acquisition of all major taxa present within the I. ramosa microbiome, we were able to analyze the functional potential of a sponge-associated microbial community in unprecedented detail. Critical functions, such as carbon fixation, which had previously only been assigned to a restricted set of sponge-associated organisms, were actually spread across diverse symbiont taxa, whereas other essential pathways, such as ammonia oxidation, were confined to specific keystone taxa.

Effects of depth and turbidity on the in situ pumping activity of the Mediterranean sponge Chondrosia reniformis (Nardo, 1847) were characterized by measuring osculum diameter, oscular outflow velocity, osculum density per sponge and sponge surface area at different locations around the Bodrum peninsula (Turkey). Outflow velocity was measured using a new method based on video analysis of neutrally buoyant particles moving in the exhalant stream of sponge oscula, which yielded results that were in good comparison to other studies. Using the new method, it was shown that for C. reniformis, oscular outflow had a location-dependent, in most cases positive relationship with oscular size: bigger oscules process more water per cm2 of osculum surface. Turbidity and depth both affected sponge pumping in a negative way, but for the locations tested, the effect of depth was more profound than the effect of turbidity. Depth affected all parameters investigated except sponge size, whereas turbidity only affected specific pumping rates normalized to sponge surface area. Deep water sponges had clearly smaller oscula than shallow water sponges, but partially compensated for this lower pumping potential by showing a higher osculum density. Both increasing turbidity and increasing depth considerably decreased volumetric pumping rates of C. reniformis. These findings have important implications for selecting sites for mariculture of this species.

Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but

Marine sponges are set to become more abundant in many near-future oligotrophic environments, where they play crucial roles in nutrient cycling. Of high importance is their mass turnover of dissolved organic matter (DOM), a heterogeneous mixture that constitutes the largest fraction of organic matter in the ocean and is recycled primarily by bacterial mediation. Little is known, however, about the mechanism that enables sponges to incorporate large quantities of DOM in their nutrition, unlike most other invertebrates. Here, we examine the cellular capacity for direct processing of DOM, and the fate of the processed matter, inside a dinoflagellate-hosting bioeroding sponge that is prominent on Indo-Pacific coral reefs. Integrating transmission electron microscopy with nanoscale secondary ion mass spectrometry, we track 15 N- and 13 C-enriched DOM over time at the individual cell level of an intact sponge holobiont. We show initial high enrichment in the filter-feeding cells of the sponge, providing visual evidence of their capacity to process DOM through pinocytosis without mediation of resident bacteria. Subsequent enrichment of the endosymbiotic dinoflagellates also suggests sharing of host nitrogenous wastes. Our results shed light on the physiological mechanism behind the ecologically important ability of sponges to cycle DOM via the recently described sponge loop.

In this study, novel methods were tested to culture the collagen-rich sponge Chondrosia reniformis Nardo, 1847 (Demospongiae, Chondrosiida, Chondrosiidae) in the proximity of floating fish cages. In a trial series, survival and growth of cultured explants were monitored near a polluted fish farm and a pristine control site. Attachment methods, plate materials, and plate orientation were compared. In a first trial, chicken wire-covered polyvinyl chloride (PVC) was found to be the most suitable substrate for C. reniformis (100% survival). During a second trial, survival on chicken wire-covered PVC, after six months, was 79% and 63% for polluted and pristine environments, respectively. Net growth was obtained only on culture plates that were oriented away from direct sunlight (39% increase in six months), whereas sponges decreased in size when sun-exposed. Chicken wire caused pressure on explants and it resulted in unwanted epibiont growth and was therefore considered to be unsuitable for long-term culture. In a final trial, sponges were glued to PVC plates and cultured for 13 months oriented away from direct sunlight. Both survival and growth were higher at the polluted site (86% survival and 170% growth) than at the pristine site (39% survival and 79% growth). These results represent a first successful step towards production of sponge collagen in integrated aquacultures.

Successful dispersal of freshwater sponges depends on the formation of dormant sponge bodies (gemmules) under adverse conditions. Gemmule formation allows the sponge to overcome critical environmental conditions, for example, desiccation or freezing, and to re-establish as a fully developed sponge when conditions are more favorable. A key process in sponge development from hatched gemmules is the construction of the silica skeleton. Silica spicules form the structural support for the three-dimensional filtration system the sponge uses to filter food particles from ambient water. We studied the effect of different hypergravity forces (1, 2.5, 5, 10, and 20 × g for 48 h)—as measure for environmental stress—on the ability of developing sponges to set-up their spiculous skeleton. Additionally, we assessed whether the addition of nutrients (i.e., dissolved 13C- and 15N-labeled amino acids) compensates for this stress. Our results show that freshwater sponges can withstand prolonged periods of hypergravity exposure and successfully set-up their skeleton, even after 48 h under 20 × g. Developing sponges were found to take up and assimilate dissolved food before forming a functional filtering system. However, fed and non-fed sponges showed no differences in skeleton formation and relative surface area growth, suggesting that the gemmules’ intrinsic energy fulfills the processes of skeleton construction. Additionally, non-fed sponges formed oscula significantly more often than fed sponges, especially under higher g-forces. This suggests that the eventual formation of a filtration system might be stimulated by food deprivation and environmentally stressful conditions. These findings indicate that the process of spiculous skeleton formation is energy-efficient and highly resilient. The uptake of dissolved food substances by freshwater sponges may contribute to the cycling of dissolved organic matter in freshwater ecosystems where sponges are abundant.

Regeneration is an essential process for all multicellular organisms, allowing them to recover effectively from internal and external injury. This process has been studied extensively in a medical context in vertebrates, with pathways often investigated mechanistically, both to derive increased understanding and as potential drug targets for therapy. Several species from other parts of the metazoan tree of life, noted for their regenerative prowess, have previously been targeted for study. This allows us to understand their regenerative mechanisms and see how they could be adapted for use in medicine. Species in clades such asHydra,planarians and echinoderms can regenerate large portions of their body, the former two clades being able to completely regenerate from even a small portion of their somatic tissue. Less well-documented for their regenerative abilities are sponges. This is surprising, as they are both one of the earliest-branching extant metazoan phyla on Earth, and are rapidly able to respond to injury. Their sessile lifestyle, lack of an external protective layer, inability to respond to predation and filter-feeding strategy all mean that regeneration is often required. In particular the demosponge genusHalisarcahas been noted for its fast cell turnover and ability to quickly adjust its cell kinetic properties to repair damage through regeneration. However, while the rate and structure of regeneration in sponges has begun to be investigated, the molecular mechanisms behind this ability are yet to be catalogued.Here we describe the assembly of a reference transcriptome forHalisarca caerulea,along with additional transcriptomes noting response to injury before, shortly following (2 hrs post-), and 12 hrs after trauma. RNAseq reads were assembled using Trinity, annotated, and samples compared, to allow initial insight into the transcriptomic basis of sponge regenerative processes. These resources are deep, with our reference assembly containing more than 92.6% of the BUSCO Metazoa set of genes, and well-assembled (N50s of 836, 957, 1,688 and 2,032 for untreated, 2h, 12h and reference transcriptomes respectively), and therefore represent excellent initial resources as a bedrock for future study. The generation of transcriptomic resources from sponges before and following deliberate damage has allowed us to study particular pathways within this species responsible for repairing damage. We note particularly the involvement of the Wnt cascades in this process in this species, and detail the contents of this cascade, along with cell cycle, extracellular matrix and apoptosis-linked genes in this work.This resource represents an excellent starting point for the continued development of this knowledge, givenH. caerulea’s ability to regenerate and position as an outgroup for comparing the process of regeneration across metazoan lineages. With this resource in place, we can begin to infer the regenerative capacity of the common ancestor of all extant animal life, and unravel the elements of regeneration in an often-overlooked clade.

Corals and macroalgae release large quantities of dissolved organic matter (DOM), one of the largest sources of organic matter produced on coral reefs. By rapidly taking up DOM and transforming it into particulate detritus, coral reef sponges are proposed to play a key role in transferring the energy and nutrients in DOM to higher trophic levels via the recently discovered sponge loop. DOM released by corals and algae differs in quality and composition, but the influence of these different DOM sources on recycling by the sponge loop has not been investigated. Here, we used stable isotope pulse-chase experiments to compare the processing of naturally sourced coral- and algal-derived DOM by three Red Sea coral reef sponge species: Chondrilla sacciformis, Hemimycale arabica and Mycale fistulifera. Incubation experiments were conducted to trace 13C- and 15N-enriched coral- and algal-derived DOM into the sponge tissue and detritus. Incorporation of 13C into specific phospholipid-derived fatty acids (PLFAs) was used to differentiate DOM assimilation within the sponge holobiont (i.e. the sponge host vs. its associated bacteria). All sponges assimilated both coral- and algal-derived DOM, but incorporation rates were significantly higher for algal-derived DOM. The two DOM sources were also processed differently by the sponge holobiont. Algal-derived DOM was incorporated into bacteria-specific PLFAs at a higher rate while coral-derived DOM was more readily incorporated into sponge-specific PLFAs. A substantial fraction of the dissolved organic carbon (C) and nitrogen (N) assimilated by the sponges was subsequently converted into and released as particulate detritus (15–24% C and 27–49% N). However, algal-derived DOM was released as detritus at a higher rate. The higher uptake and transformation rates of algal- compared with coral-derived DOM suggest that reef community phase shifts from coral to algal dominance may stimulate DOM cycling through the sponge loop with potential consequences for coral reef biogeochemical cycles and food webs.

Here we report on the trophodynamics of the bacteria-containing coral reef sponge Halisarca caerulea. The assimilation and respiration of the 13C-enriched substrates glucose, algal-derived dissolved and particulate organic matter (diatom-DOM and -POM), and bacteria were followed in 1- and 6-h incubations. Except for glucose, all substrates were readily processed by the sponge, with assimilation being the major fate. 13C-Enrichment patterns in fatty acid biomarkers revealed that sponge dissolved organic 13C assimilation was both direct and bacteria mediated as tracer carbon was recovered both in bacteria-specific and nonbacterial fatty acid. This is the first direct evidence of DOM incorporation by sponges. The present study demonstrates that the encrusting sponge H. caerulea feeds on both DOM and POM and given their dominant coverage of the largest coral reef habitat (coral cavities) it is proposed that organic matter assimilation by cryptic reef sponges may represent an important, largely overlooked ecological function. Quantitatively significant DOM processing may not be the exclusive function of the microbial world on coral reefs; sponges transform DOM to biomass, and thus retain and store organic matter in the reef system.

We studied the removal of dissolved organic carbon (DOC) and bacterioplankton by the encrusting sponges Halisarca caerulea, Mycale microsigmatosa and Merlia normani in coral reefs along Curacao, Netherlands Antilles. Sponge specimens were collected from coral reef cavities and incubations were done on the fore-reef slope at 12 m depth. The concentrations of DOC and bacteri- oplankton carbon (BC) were monitored in situ, using incubation chambers with sponges and without sponges (incubations with coral rock or ambient reef water only). Average (±SD) DOC removal rates (in μmol C cm -3 sponge h -1 ) amounted to 13.1 ± 2.5, 15.2 ± 0.9 and 13.6 ± 2.4 for H. caerula, M. micro- sigmatosa and M. normani, respectively. The DOC removal rates by the 3 sponges were on average 2 orders of magnitude higher than BC removal rates and accounted for more than 90% of the total organic carbon removal. Total organic carbon removal rates presented here were the highest ever reported for sponges. In an additional experiment with H. caerulea, the fate of organic carbon was reconstructed by measuring dissolved oxygen (O2) removal and dissolved inorganic carbon (DIC) release in a laminar flow chamber. H. caerulea respired 39 to 45% of the organic carbon removed. The remaining 55 to 61% of carbon is expected to be assimilated. We argue that H. caerulea may have a rapid turnover of matter. All 3 sponge species contained associated bacteria, but it is unclear to what extent the associated bacteria are involved in the nutrition of the sponge. We conclude that the 3 sponge-microbe associations are (related to the availability of dissolved and particulate carbon sources in the ambient water) 'dissolved organic matter (DOM)-feeders' and encrusting sponges are of quantitative importance in the removal of DOC in coral reef cavities.

Shallow warm-water and deep-sea cold-water corals engineer the coral reef framework and fertilize reef communities by releasing coral mucus, a source of reef dissolved organic matter (DOM). By transforming DOM into particulate detritus, sponges play a key role in transferring the energy and nutrients in DOM to higher trophic levels on Caribbean reefs via the so-called sponge loop. Coral mucus may be a major DOM source for the sponge loop, but mucus uptake by sponges has not been demonstrated. Here we used laboratory stable isotope tracer experiments to show the transfer of coral mucus into the bulk tissue and phospholipid fatty acids of the warm-water sponge Mycale fistulifera and cold-water sponge Hymedesmia coriacea, demonstrating a direct trophic link between corals and reef sponges. Furthermore, 21–40% of the mucus carbon and 32–39% of the nitrogen assimilated by the sponges was subsequently released as detritus, confirming a sponge loop on Red Sea warm-water and north Atlantic cold-water coral reefs. The presence of a sponge loop in two vastly different reef environments suggests it is a ubiquitous feature of reef ecosystems contributing to the high biogeochemical cycling that may enable coral reefs to thrive in nutrient-limited (warm-water) and energy-limited (cold-water) environments.

We studied the removal of dissolved organic carbon (DOC) by coral cavities of 50-250 dm3 at a depth range of 5-17 m along the coral reefs of Curacao, Netherlands Antilles, and the Berau area, East Kalimantan, Indonesia. We found significantly lower DOC concentrations in cavity water compared with ambient reef water. On average, DOC concentrations in cavity water were 15.1 ± 6.0 µmol L−1 (Curacao) and 4.0 ± 2.4 µmol L−1 (Berau) lower than in reef water. When the cavities were closed, DOC concentrations in the cavities declined by 22% ± 8% and 11% ± 4% in Curacao and Berau, respectively, within 30 min. This corresponded to average DOC removal rates per cavity surface area of 342 ± 82 mmol C m−2 d−1 in Curacao and 90 ± 45 mmol C m−2 d−1 in Berau. Bioassays showed that bacterioplankton are not responsible for this DOC removal by coral cavities. DOC fluxes exceeded bacterioplankton carbon (BC) fluxes into cavities by two orders of magnitude. On average BC fluxes per cavity surface area were 3.6 ± 1.3 mmol C m−2 d−1 (Curacao) and 1.9 ± 1.3 mmol C m−2 d−1 (Berau area). The net DOC removal per square meter of cryptic surface likely exceeded the gross primary production per square meter of planar reef area. We conclude that coral cavities and their biota are net sinks of DOC and play an important role in the energy budget of coral reefs.

Sponge Pump “Darwin's Paradox” asks how productive and diverse ecosystems like coral reefs thrive in the marine equivalent of a desert. De Goeij et al. (p. 108 ) now show that coral reef sponges are part of a highly efficient recycling pathway for dissolved organic matter (DOM), converting it, via rapid sponge-cell turnover, into cellular detritus that becomes food for reef consumers. DOM transfer through the sponge loop approaches the gross primary production rates required for the entire coral reef ecosystem.

Alexander, Brittany E. et. al.-- 11 pages, 5 figures, 2 tables, supporting information http://dx.doi.org/10.1371/journal.pone.0109486.s001 https://doi.org/10.1371/journal.pone.0109486.s002, This study describes in vivo cell turnover (the balance between cell proliferation and cell loss) in eight marine sponge species from tropical coral reef, mangrove and temperate Mediterranean reef ecosystems. Cell proliferation was determined through the incorporation of 5-bromo-29-deoxyuridine (BrdU) and measuring the percentage of BrdU-positive cells after 6 h of continuous labeling (10 h for Chondrosia reniformis). Apoptosis was identified using an antibody against active caspase-3. Cell loss through shedding was studied quantitatively by collecting and weighing sponge-expelled detritus and qualitatively by light microscopy of sponge tissue and detritus. All species investigated displayed substantial cell proliferation, predominantly in the choanoderm, but also in the mesohyl. The majority of coral reef species (five) showed between 16.1615.9% and 19.062.0% choanocyte proliferation (mean6SD) after 6 h and the Mediterranean species, C. reniformis, showed 16.663.2% after 10 h BrdU-labeling. Monanchora arbuscula showed lower choanocyte proliferation (8.163.7%), whereas the mangrove species Mycale microsigmatosa showed relatively higher levels of choanocyte proliferation (70.566.6%). Choanocyte proliferation in Haliclona vansoesti was variable (2.8-73.1%). Apoptosis was negligible and not the primary mechanism of cell loss involved in cell turnover. All species investigated produced significant amounts of detritus (2.5-18% detritus bodyweight21?d21) and cell shedding was observed in seven out of eight species. The amount of shed cells observed in histological sections may be related to differences in residence time of detritus within canals. Detritus production could not be directly linked to cell shedding due to the degraded nature of expelled cellular debris. We have demonstrated that under steady-state conditions, cell turnover through cell proliferation and cell shedding are common processes to maintain tissue homeostasis in a variety of sponge species from different ecosystems. Cell turnover is hypothesized to be the main underlying mechanism producing sponge-derived detritus, a major trophic resource transferred through sponges in benthic ecosystems, such as coral reefs. © 2014 Alexander et al., Porifarma B.V. received funding from the European Union Seventh Framework Programme (FP7/2007–2013) under grant agreement no. KBBE-2010– 266033 to undertake the research leading to these results. Funding was also received from The Innovational Research Incentives Scheme of the Netherlands Organization for Scientific Research (NWO-VENI; 863.10.009; personal grant to JMdG). Mediterranean sampling was partially funded by the grant CGL2010–18466 from the Spanish Government to MR. BEA, RO, and JMdG are affiliated with Porifarma B.V. Porifarma B.V. provided support in the form of salaries for authors BEA, RO, and JMdG, but no employees of Porifarma B.V. other than BEA, RO, and JMdG had any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript

7 pages, 3 figures, 2 tables, Coral-excavating sponges are the most important bioeroders on Caribbean reefs and increase in abundance throughout the region. This increase is commonly attributed to a concomitant increase in food availability due to eutrophication and pollution. We therefore investigated the uptake of organic matter by the two coral-excavating sponges Siphonodictyon sp. and Cliona delitrix and tested whether they are capable of consuming dissolved organic carbon (DOC) as part of their diet. A device for simultaneous sampling of water inhaled and exhaled by the sponges was used to directly measure the removal of DOC and bacteria in situ. During a single passage through their filtration system 14% and 13% respectively of the total organic carbon (TOC) in the inhaled water was removed by the sponges. 82% (Siphonodictyon sp.; mean±SD; 13±17 μmol L-1) and 76% (C. delitrix; 10±12 μmol L-1) of the carbon removed was taken up in form of DOC, whereas the remainder was taken up in the form of particulate organic carbon (POC; bacteria and phytoplankton) despite high bacteria retention efficiency (72±15% and 87±10%). Siphonodictyon sp. and C. delitrix removed DOC at a rate of 461±773 and 354±562 mmol C h-1 respectively. Bacteria removal was 1.8±0.9×1010 and 1.7±0.6×1010 cells h-1, which equals a carbon uptake of 46.0±21.2 and 42.5±14.0 μmol C h-1 respectively. Therefore, DOC represents 83 and 81% of the TOC taken up by Siphonodictyon sp. and C. delitrix per hour. These findings suggest that similar to various reef sponges coral-excavating sponges also mainly rely on DOC to meet their carbon demand. We hypothesize that excavating sponges may also benefit from an increasing production of more labile algal-derived DOC (as compared to coral-derived DOC) on reefs as a result of the ongoing coral-algal phase shift. © 2014 Mueller et al., The research leading to these results has received funding from the European Union Seventh Framework Programme (P7/2007-2013) under grant agreement no 244161 (Future of Reefs in a Changing Environment) and the Innovational Research Incentives Scheme of the Netherlands Organization for Scientific Research (NWO-VENI; 863.10.009; pers. grant to JMdG)

Sponges are important ecological and functional components of coral reefs. Recently, a new hypothesis about the functional ecology of sponges in organic matter recycling pathways, the sponge‐loop hypothesis, in which dissolved and particulate organic matter is taken up by sponges and shunted to higher trophic levels as detritus, has been proposed and demonstrated for shallow (Halisarca caerulea from water depths of 10 and 50 m. Detritus production was significantly lower in mesophotic sponges compared to shallow samples of H. caerulea. Additionally, detritus production rates in transplanted sponges moved in the direction of rates observed for resident conspecifics. The microbiome of these sponge populations was also significantly different between shallow and mesophotic depths, and the microbial communities of the transplanted sponges also shifted in the direction of their new depth in 10 d largely driven by changes in Oxyphotobacteria, Acidimicrobiia, Nitrososphaeria, Nitrospira, Deltaproteobacteria, and Dadabacteriia. This occurred in an environment where the availability of both dissolved and particulate trophic resources changed significantly across the shallow to mesophotic depth gradient where these sponge populations were found. These results suggest that changes in sponge detritus production are primarily driven by differential quality and quantity of trophic resources, as well as their utilization by the sponge host, and its microbiome, along the shallow to mesophotic depth gradient.

Sponges possess exceptionally diverse associated microbial communities and play a major role in (re)cycling of dissolved organic matter (DOM) in marine ecosystems. Linking sponge-associated community structure with DOM utilization is essential to understand host–microbe interactions in the uptake, processing, and exchange of resources. We coupled, for the first time, DNA-stable isotope probing (DNA-SIP) with 16S rRNA amplicon sequencing in a sponge holobiont to identify which symbiotic bacterial taxa are metabolically active in DOM uptake. Parallel incubation experiments with the sponge Plakortis angulospiculatus were amended with equimolar quantities of unlabelled (12C) and labelled (13C) DOM. Seven bacterial amplicon sequence variants (ASVs), belonging to the phyla PAUC34f, Proteobacteria, Poribacteria, Nitrospirae, and Chloroflexi, were identified as the first active consumers of DOM. Our results support the predictions that PAUC34f, Poribacteria, and Chloroflexi are capable of organic matter degradation through heterotrophic carbon metabolism, while Nitrospirae may have a potential mixotrophic metabolism. We present a new analytical application of DNA-SIP to detect substrate incorporation into a marine holobiont with a complex associated bacterial community and provide new experimental evidence that links the identity of diverse sponge-associated bacteria to the consumption of DOM.

This document is the work of a team assembled by the International Coral Reef Society (ICRS). The mission of ICRS is to promote the acquisition and dissemination of scientific knowledge to secure the future of coral reefs, including via relevant policy frameworks and decision-making processes. This document seeks to highlight the urgency of taking action to conserve and restore reefs through protection and management measures, to provide a summary of the most relevant and recent natural and social science that provides guidance on these tasks, and to highlight implications of these findings for the numerous discussions and negotiations taking place at the global level.