Chondrilla Nucula Research Articles

High microbiome and metabolome diversification in coexisting sponges with different bio-ecological traits

Marine Porifera host diverse microbial communities, which influence host metabolism and fitness. However, functional relationships between sponge microbiomes and metabolic signatures are poorly understood. We integrate microbiome characterization, metabolomics and microbial predicted functions of four coexisting Mediterranean sponges –Petrosia ficiformis, Chondrosia reniformis, Crambe crambe and Chondrilla nucula. Microscopy observations reveal anatomical differences in microbial densities. Microbiomes exhibit strong species-specific trends. C. crambe shares many rare amplicon sequence variants (ASV) with the surrounding seawater. This suggests important inputs of microbial diversity acquired by selective horizontal acquisition. Phylum Cyanobacteria is mainly represented in C. nucula and C. crambe. According to putative functions, the microbiome of P. ficiformis and C. reniformis are functionally heterotrophic, while C. crambe and C. nucula are autotrophic. The four species display distinct metabolic profiles at single compound level. However, at molecular class level they share a “core metabolome”. Concurrently, we find global microbiome-metabolome association when considering all four sponge species. Within each species still, sets of microbe/metabolites are identified driving multi-omics congruence. Our findings suggest that diverse microbial players and metabolic profiles may promote niche diversification, but also, analogous phenotypic patterns of “symbiont evolutionary convergence” in sponge assemblages where holobionts co-exist in the same area.

Effect of Acute Thermal Stress Exposure on Ecophysiological Traits of the Mediterranean Sponge Chondrilla nucula: Implications for Climate Change.

As a result of climate change, the Mediterranean Sea has been exposed to an increase in the frequency and intensity of marine heat waves in the last decades, some of which caused mass mortality events of benthic invertebrates, including sponges. Sponges are an important component of benthic ecosystems and can be the dominant group in some rocky shallow-water areas in the Mediterranean Sea. In this study, we exposed the common shallow-water Mediterranean sponge Chondrilla nucula (Demospongiae: Chondrillidae) to six different temperatures for 24 h, ranging from temperatures experienced in the field during the year (15, 19, 22, 26, and 28 °C) to above normal temperatures (32 °C) and metabolic traits (respiration and clearance rate) were measured. Both respiration and clearance rates were affected by temperature. Respiration rates increased at higher temperatures but were similar between the 26 and 32 °C treatments. Clearance rates decreased at temperatures >26 °C, indicating a drop in food intake that was not reflected by respiration rates. This decline in feeding, while maintaining high respiration rates, may indicate a negative energy balance that could affect this species under chronic or repeated thermal stress exposure. C. nucula will probably be a vulnerable species under climate change conditions, affecting its metabolic performance, ecological functioning and the ecosystem services it provides.

Evaluation of metallic pollution of north eastern Algerian coasts using the demosponge Chondrilla nucula Schmidt, 1862

Evaluation of metallic pollution of north eastern Algerian coasts using the demosponge Chondrilla nucula Schmidt, 1862

Photosynthetic Sponge-associated Eukaryotes in the Aegean Sea: A Culture-dependent Approach.

Symbioses between sponges and photosynthetic organisms are very diverse regarding the taxonomy and biogeography of both hosts and symbionts; to date, most research has focused on the exploration of bacterial diversity. The present study aims to characterize the culturable diversity of photosynthetic eukaryotes associated with sponges in the Aegean Sea, on which no information exists. Five microalgae strains were isolated from marine sponges; the strains were characterized by morphological features, and the 18S rRNA, 18S-28S Internal Transcribed Spacer, and ribulose-bisphosphate carboxylase large chain (rbcL) sequences. Our polyphasic approach showed that the strains belonged to the green-alga Acrochaete leptochaete, the diatom Nanofrustulum cf. shiloi, the rhodophyte Acrochaetium spongicola, and the chlorachniophyte Lotharella oceanica. A.leptochaete is reported for the first time in sponges, even though green algae are known to be associated with sponges. Nanofrustulum shiloi was found in association with the sponges Agelas oroides and Chondrilla nucula, whereas information existed only for its association with the species Aplysina aerophoba. Acrochaetium spongicola was found for the first time in association with sponges in the eastern Mediterranean. Moreover, we report herein for the first time a sponge-chlorarachniophycean association. Our research revealed new diversity of microalgae associated with sponges and added new records of sponge species, previously unknown for their association with microalgae.

Niche partitioning between sea turtles in waters of a protected tropical island

Juvenile sea turtles recruit in coastal areas where they act as habitat engineers modifying the coastal landscape through feeding. However, little is known about the coexistence of these mega-vertebrates and their potential competition for resources. In this work, diet, food selectivity, trophic niche width and niche overlap of juveniles of two sympatric sea turtle species (Eretmochelys imbricata and Chelonia mydas) were evaluated from gastric lavages and habitat surveys in a tropical island bay of the southwestern Atlantic. The main items selected by E. imbricata were the zoanthid Zoanthus sociatus, the sponge Chondrilla nucula and red algae while C. mydas showed strong selectivity for red algae, mainly Asparagopsis sp. Species diets differed significantly and niche overlap was low; E. imbricata’s recorded niche was 2.5 times larger than that of C. mydas. We conclude that these two species do not compete for food in a well-preserved environment and that their feeding habits provide favorable conditions for local corals and other benthic groups to prosper by means of foraging on coral-competitors.

Comparative study on Hg bioaccumulation and biotransformation in Mediterranean and Atlantic sponge species

In this work we present an assessment of mercury (Hg) and methyl mercury (MeHg) bioaccumulation in different species of marine sponges collected off the Northwestern Mediterranean and Northeastern Atlantic coasts. Overall the results showed significant accumulation of Hg in sponges, with the Mediterranean sponge Chondrilla nucula exhibiting the highest total Hg content (up to 0.5 mg kg−1) and bio-concentration factor (BCF) up to 23. A significant inter-species variability of Hg bioaccumulation was observed among species collected at the same site. The sponges, collected in marine environment contaminated with Hg show consistently higher Hg accumulation, meaning that the bioaccumulation is proportional to the Hg availability in the surrounding environment. Different extraction protocols were tested for MeHg analysis and, generally, a low MeHg ratio in Hg species (4% and 17% average for Mediterranean and Irish sponges respectively) was detected suggesting a possible demethylation process and therefore a promising role of sponges for Hg bioremediation Additionally, the Hg isotopic composition in these organisms was determined and it showed that MDF (mass dependent fractionation) is the main process in sponges, with the absence of significant MIF. This result suggests a dominant role of associated microbial population in the methylation and/or demethylation processes.

Leptothoe, a new genus of marine cyanobacteria (Synechococcales) and three new species associated with sponges from the Aegean Sea

Cyanobacterial diversity associated with sponges remains underestimated, though it is of great scientific interest in order to understand the ecology and evolutionary history of the symbiotic relationships between the two groups. Of the filamentous cyanobacteria, the genus Leptolyngbya is the most frequently found in association with sponges as well as the largest and obviously polyphyletic group. In this study, five Leptolyngbya-like sponge-associated isolates were investigated using a combination of molecular, chemical, and morphological approach and revealed a novel marine genus herein designated Leptothoe gen. nov. In addition, three new species of Leptothoe, Le.sithoniana, Le.kymatousa, and Le.spongobia, are described based on a suite of distinct characters compared to other marine Leptolyngbyaceae species/strains. The three new species, hosted by four sponge species, showed different degrees of host specificity. Leptothoe sithoniana and Le.kymatousa hosted by the sponges Petrosia ficiformis and Chondrilla nucula, respectively, seem to be more specialized than Le.spongobia, which was hosted by the sponges Dysidea avara and Acanthella acuta. All three species contained nitrogen-fixing genes and may contribute to the nitrogen budget of sponges. Leptothoe spongobia TAU-MAC 1115 isolated from Acanthella acuta was shown to produce microcystin-RR indicating that microcystin production among marine cyanobacteria could be more widespread than previously determined.

Genome Sequence of the Halophilic Bacterium Kangiella spongicola ATCC BAA-2076T.

The Gram-negative genus Kangiella contains a number of halophilic species that display high levels of iso-branched fatty acids. Kangiella spongicola was isolated from a marine sponge, Chondrilla nucula, from the Florida Keys in the United States. A genome assembly of 2,825,399 bp with a 44.31% G+C content was generated from strain A79T (=ATCC BAA-2076T).

Marine sponges as a powerful tool for trace elements biomonitoring studies in coastal environment

In this work, we performed a comparative study on six marine sponge species collected along the French Mediterranean and Irish coasts for their TEs accumulation. Intra and inter-species variabilities were examined. Among the Mediterranean species, Cymbaxinella damicornis accumulates significantly more As and Cu than others sponge species; Chondrilla nucula more Ni and Mo and Acanthella acuta more Ag. Among Irish samples, Hymeniacidon perlevis showed higher accumulation properties for most of TEs in comparison to Halichondria panicea. Bioconcentration Factors were > 1 in all species for most of TEs. This study suggests that TEs bioaccumulation is most likely associated to differences in morphological features and/or to specific bacterial communities associated to different species. The determination of Pb isotope ratios revealed mainly natural Pb sources for Mediterranean and Kilkieran Bay's samples, and rather anthropogenic influence for Belfast samples. This study confirms that sponges represent a powerful tool for biomonitoring studies.

In vivo exposure of the marine sponge Chondrilla nucula Schmidt, 1862 to cadmium (Cd), copper (Cu) and lead (Pb) and its potential use for bioremediation purposes

The study aimed to test the cadmium (Cd), copper (Cu) and lead (Pb) bioaccumulation capacity of the marine sponge Chondrilla nucula and to measure the expression of metallothioneins (MTs) by a western blotting assay to explore metal tolerance and its potential use as a bioremediator in contaminated coastal areas. C. nucula was sampled in a protected marine area in order to perform experiments on organisms living in a healthy environment.Under laboratory conditions, the sponges were exposed to increasing concentrations of Cd, Cu and Pb in tanks filled with artificial seawater set up for the experiments. For each metal, three waterborne concentrations (mgL−1) of Cd (0.02–0.04-0.08), Cu (0.1–0.2-0.4) and Pb (0.2–0.4-0.8) were considered separately. SPSS 20.0 was used for statistical analysis. Significant differences in bioaccumulation across levels of each metal were highlighted. Moreover, the amount accumulated in sponges increased proportionately with increasing levels of exposure for each metal as well as MT expression after Cd and Pb exposure.The results demonstrate the efficiency of C. nucula in accumulating high levels of Cu, but a low tolerance to progressively higher concentrations for Cd and Pb. The study suggests the suitability of the use of this species in bioremediation plans for moderately contaminated environments. However, the biological response in the field should be verified by the use of transplanted organisms from a control site to a polluted site.

Phenolic bisabolanes from the sponge-derived fungus Aspergillus sp.

Two new phenolic bisabolane sesquiterpenes, asperchondols A (1) and B (2), together with seven known analogues (3–9) and four known diphenyl ethers (10–13) were obtained from Aspergillus sp., that had been isolated from the marine sponge Chondrilla nucula. Their structures were elucidated through NMR and MS analysis, and by comparison with literature data. All isolated compounds were evaluated for their antibacterial activity against eight human pathogenic bacteria. Co-cultivation experiment of Aspergillus sp. with Bacillus subtilis was also conducted.

Effects of ocean acidification on sponge communities

AbstractThe effects of ocean acidification on lower invertebrates such as sponges may be pronounced because of their low capacity for acid–base regulation. However, so far, most studies have focused on calcifiers. We present the first study of the effects of ocean acidification on the Porifera. Sponge species composition and cover along pH gradients at CO2 vents off Ischia (Tyrrhenian Sea, Italy) was measured at sites with normal pH (8.1–8.2), lowered pH (mean 7.8–7.9, min 7.4–7.5) and extremely low pH (6.6). There was a strong correlation between pH and both sponge cover and species composition. Crambe crambe was the only species present in any abundance in the areas with mean pH 6.6, seven species were present at mean pH 7.8–7.9 and four species (Phorbas tenacior, Petrosia ficiformis, Chondrilla nucula and Hemimycale columella) were restricted to sites with normal pH. Sponge percentage cover decreased significantly from normal to acidified sites. No significant effect of increasing CO2 levels and decreasing pH was found on spicule form in Crambe crambe. This study indicates that increasing CO2 concentrations will likely affect sponge community composition as some demosponge species appear to be more vulnerable than others. Further research into the mechanisms by which acidification affects sponges would be useful in predicting likely effects on sessile marine communities.

Foraging Selectivity of the Hawksbill Sea Turtle (Eretmochelys imbricata) in the Culebra Archipelago, Puerto Rico

Recent literature on foraging in Hawksbill Sea Turtles in the Caribbean region concludes that prey selectivity is a combination of preference for certain prey species and their local abundance. In this study, prey selectivity patterns were measured in five juvenile Hawksbill Sea Turtle (Eretmochelys imbricata) aggregations in the Culebra Archipelago, Puerto Rico, and the hypothesis that juvenile Hawksbill Sea Turtles exhibit selectivity for certain prey items independent of their environmental availability was tested. Hawksbill Sea Turtles showed positive selection for the corallimorph Ricordea florida, which was rare in all four study sites, and for the alga Lobophora variegata, that was abundant in one site. Turtles exhibited low preference for the sponge Chondrilla nucula, the most common prey item in both diet samples and the environment at all study sites. Low preference for this sponge corresponds to its high availability in the environment. Turtles also exhibited low preference for the sponge Cinacyrella sp. and the branching anemone Lebrunia danae. That juvenile hawksbills exhibited strong positive selectivity for rare items indicates that diet selection is not necessarily related to the abundance of the items in the environment. In addition, spatial variability in diet composition among Hawksbill Sea Turtles in the Culebra Archipelago indicates plasticity in their foraging habits.

Kangiella spongicola sp. nov., a halophilic marine bacterium isolated from the sponge Chondrilla nucula

A novel halophilic bacterium of the genus Kangiella was isolated from a marine sponge collected from the Florida Keys, USA. Strain A79(T), an aerobic, Gram-negative, non-motile, rod-shaped bacterium, grew in 2-15 % (w/v) NaCl, at a temperature of 10-49 °C and at pH 4.5-10. Phylogenetic analysis placed strain A79(T) in the family Alcanivoraceae in the class Gammaproteobacteria. Strain A79(T) showed 98.5 % 16S rRNA gene sequence similarity to Kangiella japonica KMM 3899(T), 96.6 % similarity to Kangiella koreensis DSM 16069(T) and 95.6 % similarity to Kangiella aquimarina DSM 16071(T). The major cellular fatty acids were iso-C(11 : 0), iso-C(11 : 0) 3-OH, iso-C(15 : 0), iso-C(17 : 0) and iso-C(17 : 1)ω9c and the G+C content of the genomic DNA was 44.9 mol%. On the basis of physiological, chemotaxonomic and phylogenetic comparisons, strain A79(T) represents a novel species in the genus Kangiella, for which the name Kangiella spongicola sp. nov. is proposed. The type strain is A79(T) ( = ATCC BAA-2076(T) = DSM 23219(T)).

Assessing anti-predatory chemical defences among ten eastern Mediterranean sponges

The palatability of organic chemical extracts from ten of the most abundant sponge species along the Israeli (shallow) coast, eastern Mediterranean Sea (Axinella sp., Axinella polypoides, Chondrilla nucula, Ircinia sp., Psammocinia sp. 1, Psammocinia sp. 2, Psammocinia sp. 3, Psammocinia sp. 4, Sarcotragus sp. and Tetilla sp.) was tested. To examine the generality of the phenomenon, it was evaluated with two types of potential predators, a fish and a gastropod. It was determined that the extracts of only two species (Psammocinia sp. 1 and Psammocinia sp. 3) deterred feeding of the omnivorous ornate Mediterranean wrasse Thalassoma pavo. On the other hand, extracts of five other sponges (Chondrilla nucula, Axinella sp., Ircinia sp., Sarcotragus sp. and Psammocinia sp. 2) were non-palatable to the omnivorous gastropod Strombus persicus (the extracts that deterred the fish did not deter the gastropod and vice versa). We also determined the capacity of extracts from six Red Sea sponges to deter T. pavo, and compared it with these extracts' effect on the Red Sea wrasse T. klunzingeri. All the extracts that deterred the Red Sea wrasse (from Amphimedon chloros, Crella cyatophora, Negombata magnifica and Theonella swinhoei) were also non-palatable to the Mediterranean wrasse. In addition to these four species, also Diacarnus erythraenus deterred Thalassoma pavo while being palatable to T. klunzingeri, whereas food pellets with extracts of Niphates rowi were eaten by both wrasse species.

Intergenerational transmission of symbiotic bacteria in oviparous and viviparous demosponges, with emphasis on intracytoplasmically-compartmented bacterial types

Recent molecular detection of vast microbial communities exclusively associated with sponges has made evident the need for a better understanding of the mechanisms by which these symbiotic microbes are handled and transferred from one sponge generation to another. This transmission electron microscopy (TEM) study investigated the occurrence of symbiotic bacteria in free-swimming larvae of two viviparous species (Haliclona caerulea and Corticium candelabrum) and spawned gametes of two oviparous species (Chondrilla nucula and Petrosia ficiformis). Complex microbial communities were found in these sponges, which in two cases included bacteria characterized by an intra-cytoplasmic membrane (ICM). When ICM-bearing and ICM-lacking bacteria co-existed, they were transferred following identical pathways. Nevertheless, the mechanism for microbial transference varied substantially between species. In C. nucula, a combination of intercellular symbiotic ICM-bearing and ICM-lacking bacteria, along with cyanobacteria and yeasts, were collected from the mesohyl by amoeboid nurse cells, then transported and transferred to the oocytes. In the case of Corticium candelabrum, intercellular bacteria did not enter the gametes, but spread into the division furrows of early embryos and proliferated in the central cavity of the free-swimming larva. Surprisingly, symbiotic bacteria were not vertically transmitted by P. ficiformis gametes or embryos, but apparently acquired from the environment by the juveniles of each new generation. This study failed to unravel the mechanism by which the intercellular endosymbiotic bacterium found in the central mesohyl of the H. caerulea larva got there. Nevertheless, the ultrastructure of this bacterial rod, which was characterized by a star-shaped cross section with nine radial protrusions, an ICM-bound riboplasm, and a putative membrane-bound acidocalcisome, suggested that it may represent a novel organization grade within the prokaryotes. It combines traits occurring in members of Poribacteria, Planctomycetes and Verrucomicrobia, emerging as one of the most complex prokaryotic architectures known to date.

Seasonal variation of morphological characters of Chondrilla aff. nucula (Porifera: Demospongiae) from the south-east coast of Brazil

Chondrilla nucula is a morphologically simple species defined by the presence of spherasters in its skeleton. For a long time C. nucula was considered a cosmopolitan species, however, in 1999, a molecular study demonstrated the existence of a species complex with at least four cryptic species, besides C. nucula. At that time, those four new species were not formally described because the morphological differences observed did not reflect species differences and were attributed to plasticity. Since then, researchers working on Chondrilla species suggested that the skeletal organization, the distribution of spherulous cells and the type of surface should be used to differentiate species. Individuals of Chondrilla aff. nucula from one population in Arraial do Cabo, Rio de Janeiro State, Brazil, were collected monthly and analysed in order to test the validity of those three characters to separate the species of Chondrilla. Moreover, to determine if the differences in spicule dimensions previously found were seasonal, we also quantified the diameter of the spherasters throughout the year. Our results demonstrate that all analysed characters are extremely variable and that spicule size can vary even at the same locality. The present study shows the importance of testing the variability of morphological characters before describing new species. Unfortunately, until valid taxonomic characters are found, the Atlantic Chondrilla species will have to remain undescribed.

Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge assemblages

Marine sponges are abundant and diverse components of coral reefs and commonly harbour photosynthetic symbionts in these environments. The most prevalent symbiont is the cyanobacterium, Synechococcus spongiarum, isolated from taxonomically diverse hosts from geographically distant regions. We combined analyses of chlorophyll-a (chl-a) concentrations with line-intercept transect surveys to assess the abundance and diversity of reef sponges hosting photosymbionts on Caribbean coral reefs in the Bocas del Toro Archipelago, Panamá. To identify symbionts, we designed PCR primers that specifically amplify a fragment of the 16S ribosomal RNA gene from S. spongiarum and used these primers to screen potential host sponges for the presence of this symbiont. Chlorophyll-a data divided the sponge community into two disparate groups, species with high (>125 μg/g, N=20) and low (<50 μg/g, N=38) chl-a concentrations. Only two species exhibited intermediate (50–125 μg/g) chl-a concentrations; these species represented hosts with reduced symbiont populations, including bleached Xestospongia muta and the mangrove form of Chondrilla nucula (C. nucula f. hermatypica). Sponges with high and intermediate chl-a concentrations accounted for over one-third of the species diversity and abundance of sponges in these communities. Most (85%) of these sponges harboured S. spongiarum. Molecular phylogenies reveal that S. spongiarum represents a sponge-specific Synechococcus lineage, distinct from free-living cyanobacteria. The prevalence of sponge–photosymbiont associations and dominance of symbiont communities by S. spongiarum suggest a major role of this cyanobacterium in sponge ecology and primary productivity on coral reefs.

Adaptation of reef and mangrove sponges to stress: evidence for ecological speciation exemplified by Chondrilla caribensis new species (Demospongiae, Chondrosida)

Sponges (Porifera) in mangroves have adapted to a wide range of environmental parameters except for extended periods of exposure to freshwater or air. Many marine mangrove islands are located in the shallow backwaters of coral reefs in Belize and elsewhere in the Caribbean and have a mean tidal range of only 15 cm. They are densely populated by sponges, mostly attached to subtidal red-mangrove stilt roots and peat banks lining tidal channels. Some species are endemic to mangroves, others are immigrants from nearby reefs. Mangrove endemics endure environmental hardships, such as occasional exposure to air during spring tides, temperature and salinity extremes, fine sediments, even burial in detritus. Reef immigrants into mangroves enjoy protection from spongivores that do not stray into the swamp but they eventually succumb to environmental stress. There is evidence exemplified by the common demosponge Chondrilla aff. nucula, that sponges flourishing in both mangrove and reef habitats may develop separate ecologically specialized and reproductively isolated populations. Such processes can lead to genetic modifications and thus serve as mechanisms for ecological speciation. Because Chondrilla nucula Schmidt was first described from the Mediterranean Sea, it was long suspected that the western Atlantic population may be a separate species. New morphological and molecular evidence prompt us to describe it under a new name, Chondrilla caribensis, with two ecological forms, forma caribensis from mangroves and lagoons, and forma hermatypica from open reefs.

The GABAergic‐like system in the marine demosponge Chondrilla nucula

Gamma-amino butyric acid (GABA) is believed to be the principal inhibitory neurotransmitter in the mammalian central nervous system, a function that has been extended to a number of invertebrate systems. The presence of GABA in the marine demosponge Chondrilla nucula was verified using immunofluorescence detection and high-pressure liquid chromatography. A strong GABA-like immunoreactivity (IR) was found associated with choanocytes, exopinacocytes, endopinacocytes lining inhalant, and exhalant canals, as well as in archaeocytes scattered in the mesohyl. The capacity to synthesize GABA from glutamate and to transport it into the vesicles was confirmed by the presence in C. nucula of glutamate decarboxylase (GAD) and vesicular GABA transporters (vGATs), respectively. GAD-like and vGAT-like IR show the same distribution as GABA-like IR. Supporting the similarity between sponge and mammalian proteins, bands with an apparent molecular weight of about 65-67 kDa and 57 kDa were detected using antibodies raised against mammalian GAD and vGAT, respectively. A functional metabotropic GABA(B)-like receptor is also present in C. nucula. Indeed, both GABA(B) R1 and R2 isoforms were detected by immunoblot and immunofluorescence. Also in this case, IR was found in choanocytes, exopinacocytes, and endopinacocytes. The content of GABA in C. nucula amounts to 1225.75 +/- 79 pmol/mg proteins and GABA is released into the medium when sponge cells are depolarized. In conclusion, this study is the first indication of the existence of the GABA biosynthetic enzyme GAD and of the GABA transporter vGAT in sponges, as well as the first demonstration that the neurotransmitter GABA is released extracellularly.