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During embryogenesis, organisms with lecithotrophic indirect development usually accumulate large quantities of energetic reserves in the form of yolk that are necessary for larval survival. Since all sponges have lecithotrophic development, yolk formation is an ineludible step of their embryogenesis. Sponge yolk platelets have a wide range of morphological forms, from entirely lipid or protein platelets to a combined platelet showing both lipids and proteins and even glycogen. So far, there are no comparative studies on the nature and content of yolk in congeneric species of sponges inhabiting contrasting environments, which could have putative effects on the larval adaptation to environmental conditions. Here, we have taken advantage of the worldwide distribution of the sponge genus Mycale, in order to compare the embryogenesis and yolk formation in two species inhabiting contrasting latitudinal areas: M. acerata from Antarctic waters and M. laevis from the Caribbean. We have compared their brooded embryos and larvae using scanning and transmission electron microscopy, and calculated their energetic signatures based on the nature of their yolk. While the general morphological feature of embryos and larvae of both species were very similar, the main difference resided in the yolk nature. The Antarctic species, M. acerata, showed exclusively lipid yolk, whereas the Caribbean species, M. laevis, showed combined platelets of lipids and proteins and less frequently protein yolk platelets. The larvae of M. acerata were estimated to possess a two-fold energetic signature compared to that of M. laevis, which may have important ecological implications for their survival and for maintaining large population densities in the cold waters of the Southern Ocean.

Over the past seven decades, particularly since the discovery of the first marine-derived nucleosides, spongothymidine and spongouridine, from the Caribbean sponge Cryptotethya crypta in the early 1950s, marine natural products have emerged as unique, renewable and yet under-investigated pools for discovery of new drug leads with distinct structural features, and myriad interesting biological activities. Marine sponges are the most primitive and simplest multicellular animals, with approximately 8900 known described species, although more than 15,000 species are thought to exist worldwide today. These marine organisms potentially represent the richest pipeline for novel drug leads. Mycale (Arenochalina) and Clathria are recognized marine sponge genera belonging to the order Poecilosclerida, whereas Biemna was more recently reclassified, based on molecular genetics, as a new order Biemnida. Together, these sponge genera contribute to the production of physiologically active molecular entities with diverse structural features and a wide range of medicinal and therapeutic potentialities. In this review, we provide a comprehensive insight and up-to-date literature survey over the period of 1976–2018, focusing on the chemistry of the isolated compounds from members of these three genera, as well as their biological and pharmacological activities, whenever available. © 2018 by the authors.

Bacterial specialized metabolites are increasingly recognized as important factors in animal–microbiome interactions: for example, by providing the host with chemical defenses. Even in chemically rich animals, such compounds have been found to originate from individual members of more diverse microbiomes. Here, we identified a remarkable case of a moderately complex microbiome in the sponge host Mycale hentscheli in which multiple symbionts jointly generate chemical diversity. In addition to bacterial pathways for three distinct polyketide families comprisingmicrotubule-inhibiting peloruside drug candidates, mycalamide-type contact poisons, and the eukaryotic translation-inhibiting pateamines, we identified extensive biosynthetic potential distributed among a broad phylogenetic range of bacteria. Biochemical data on one of the orphan pathways suggest a previously unknown member of the rare polytheonamide-type cytotoxin family as its product. Other than supporting a scenario of cooperative symbiosis based on bacterial metabolites, the data provide a rationale for the chemical variability of M. hentscheli and could pave the way toward biotechnological peloruside production. Most bacterial lineages in the compositionally unusual sponge microbiome were not known to synthesize bioactive metabolites, supporting the concept that microbial dark matter harbors diverse producer taxa with as yet unrecognized drug discovery potential.

Identifying cryptic species is pivotal for understanding marine biodiversity and optimizing strategies for its conservation. A robust understanding of poriferan diversity is a complex endeavour. It has also been extremely hampered by the high phenotypic plasticity and the limited number of diagnostic characters. Mycale (Carmia) cecilia has different body colours, even among individuals living together. We tested whether the colour variation could be due to polymorphism, phenotypic plasticity or cryptic speciation. Phylogenetic reconstructions of nuclear and mitochondrial loci were congruent. Individuals of different body colour did not cluster together and had high levels of genetic divergence. Furthermore, the green morphotype clustered in almost all reconstructions with Mycale (C.) phyllophila, as both showed higher gene similarity at the transcriptomic level (public transcriptome). Morphologically, the green individuals consistently showed discrepancies from the red ones. These results suggest that all individuals with the same body colour, either red or green, correspond to the same species, while individuals with different body colours probably belong to different species. These results reveal high levels of morphologic and genetic diversity, which could have important implications for what is known as M. (C.) cecilia and the Mycalidae systematics.

Background Most researches on sponge holobionts focus primarily on symbiotic microbes, yet data at the level of the sponge hologenome are still relatively scarce. Understanding of the sponge host and its microbial gene expression profiles and the host-microbes interplay in different niches represents a key aspect of sponge hologenome. Using the Hawaiian demosponge Mycale grandis in different niches as a model, i.e. on rocks, on the surface of coral Porites compressa , under alga Gracilaria salicornia , we compared the bacterial and fungal community structure, functional gene diversity, expression pattern and the host transcriptome by integrating open-format (deep sequencing) and closed-format (GeoChip microarray) high-throughput techniques. Results Little inter-niche variation in bacterial and fungal phylogenetic diversity was detected for M. grandis in different niches, but a clear niche-dependent variability in the functional gene diversity and expression pattern of M. grandis host and its symbiotic microbiota was uncovered by GeoChip microarray and transcriptome analyses. Particularly, sponge host genes related to innate immunity and microbial recognition showed a strong correlation with the microbial symbionts’ functional gene diversity and transcriptional richness in different niches. The cross-niche variability with respect to the symbiont functional gene diversity and the transcriptional richness of M. grandis holobiont putatively reflects the interplay of niche-specific selective pressure and the symbiont functional diversity. Conclusions Niche–dependent gene expression profiles of M. grandis hologenome and the host-microbes interplay were suggested though little inter-niche variation in bacterial and fungal diversity was detected, particularly the sponge innate immunity was found to be closely related to the symbiotic microbes. Altogether, these findings provide novel insights into the black box of one sponge holobiont in different niches at the hologenome level.

Despite the ecological importance and the potential pharmacological application of the sponge Mycale ( Carmia ) cecilia, it is uncertain whether the body-color variation, even in individuals coexisting in the same area, is due to intraspecific phenotypic plasticity or corresponds to taxonomic divergence. This uncertainty is relatively common in several Porifera groups, which lack the resolution of morphological diagnostic characters and slow-evolving mitochondrial genomes as occurs in early splitting lineages. We sequenced the RNA of six individuals with two different body-color (green-morphotype and red-morphotype) collected at the same time side by side. High-throughput sequencing of cDNA libraries produced ~ 129 million reads with a length of 150 bp. Each morphotype was assembled separately owing to the low overlapping in the global assembly. Metatranscriptome de novo assembly of the trimmed and normalized reads produced 461 thousand transcripts for the green-morphotype and 342 thousand for the red-morphotype (respectively). Over 30% of the transcripts contained Open Reading Frames (ORFs) with functional significance. BUSCO analysis of the ORFs of putative poriferan origin (31.3% green or 30.4% red) indicated that our assemblies are 60% complete. This is the first attempt to evaluate the morphological diversity in the species M. ( C. ) cecilia and the phylum Porifera at the transcriptomic level. Due to the minimum overlap of the assembly and that, the red-morphotype diverged significantly from the green-morphotype (original color of M. ( C. ) cecilia ). Therefore, we suggest that the red-morphotype should undergo a complete taxonomic investigation and its taxonomic status be reviewed. We expect that the transcriptome assembly metrics can be useful for comparing other transcriptome assemblies of non-model organisms.

Background Mycale cecilia is an abundant Eastern Tropical Pacific sponge living in a wide variety of habitats, including coral reefs where it may directly interact with corals. It is also known to possess secondary metabolites of pharmacological value. These aspects highlight the importance of having a better understanding of its biology, and genetic and population diversity. Methods and results In the present study, we isolated and characterized twelve novel microsatellite loci by Illumina MiSeq sequencing. The loci were tested in 30 specimens collected from two coral reef localities (La Paz, Baja California Sur and Isabel Island, Nayarit) from the Mexican Pacific using M13(-21) labeling. All loci were polymorphic, with two to nine alleles per locus. Expected heterozygosities varied from 0.616 to 0.901. Eleven loci were tested and successfully amplified in M. microsigmatosa from the Gulf of Mexico. Conclusion Here we report the first microsatellite loci developed for a sponge species from the Eastern Pacific coast. These molecular markers will be used for population genetic studies of M. cecilia , and potentially in other congeneric species; particularly in vulnerable marine areas that require protection, such as coral reefs.

Summary 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. Lay Summary

Microbial communities have a key role in the physiology of the sponge host, and it is therefore essential to understand the stability and specificity of sponge–symbiont associations. Host-specific bacterial associations spanning large geographic distance are widely acknowledged in sponges. However, the full spectrum of specificity remains unclear. In particular, it is not known whether closely related sponges host similar or very different microbiota over wide bathymetric and geographic gradients, and whether specific associations extend to the rare members of the sponge microbiome. Using the ultra-deep Illumina sequencing technology, we conducted a comparison of sponge bacterial communities in seven closely related Hexadella species with a well-resolved host phylogeny, as well as of a distantly related sponge Mycale . These samples spanned unprecedentedly large bathymetric (15–960 m) gradients and varying European locations. In addition, this study included a bacterial community analysis of the local background seawater for both Mycale and the widespread deep-sea taxa Hexadella cf. dedritifera . We observed a striking diversity of microbes associated with the sponges, spanning 47 bacterial phyla. The data did not reveal any Hexadella microbiota co-speciation pattern, but confirmed sponge-specific and species-specific host–bacteria associations, even within extremely low abundant taxa. Oligotyping analysis also revealed differential enrichment preferences of closely related Nitrospira members in closely related sponges species. Overall, these results demonstrate highly diverse, remarkably specific and stable sponge–bacteria associations that extend to members of the rare biosphere at a very fine phylogenetic scale, over significant geographic and bathymetric gradients.

During embryogenesis, organisms with lecithotrophic indirect development usually accumulate large quantities of energetic reserves in the form of yolk that are necessary for larval survival. Since all sponges have lecithotrophic development, yolk formation is an ineludible step of their embryogenesis. Sponge yolk platelets have a wide range of morphological forms, from entirely lipid or protein platelets to a combined platelet showing both lipids and proteins and even glycogen. So far, there are no comparative studies on the nature and content of yolk in congeneric species of sponges inhabiting contrasting environments, which could have putative effects on the larval adaptation to environmental conditions. Here, we have taken advantage of the worldwide distribution of the sponge genus Mycale, in order to compare the embryogenesis and yolk formation in two species inhabiting contrasting latitudinal areas: M. acerata from Antarctic waters and M. laevis from the Caribbean. We have compared their brooded embryos and larvae using scanning and transmission electron microscopy, and calculated their energetic signatures based on the nature of their yolk. While the general morphological feature of embryos and larvae of both species were very similar, the main difference resided in the yolk nature. The Antarctic species, M. acerata, showed exclusively lipid yolk, whereas the Caribbean species, M. laevis, showed combined platelets of lipids and proteins and less frequently protein yolk platelets. The larvae of M. acerata were estimated to possess a two-fold energetic signature compared to that of M. laevis, which may have important ecological implications for their survival and for maintaining large population densities in the cold waters of the Southern Ocean.