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Marine sponges have been successful in their expansion across diverse ecological niches around the globe. Pioneering work attributed this success to both a well-developed aquiferous system that allowed for efficient filter feeding on suspended organic matter and the presence of microbial symbionts that can supplement host heterotrophic feeding with photosynthate or dissolved organic carbon. We now know that sponge-microbe interactions are host-specific, highly nuanced, and provide diverse nutritional benefits to the host sponge. Despite these advances in the field, many current hypotheses pertaining to the evolution of these interactions are overly generalized; these over-simplifications limit our understanding of the evolutionary processes shaping these symbioses and how they contribute to the ecological success of sponges on modern coral reefs. To highlight the current state of knowledge in this field, we start with seminal papers and review how contemporary work using higher resolution techniques has both complemented and challenged their early hypotheses. We outline different schools of thought by discussing evidence of symbiont contribution to both host ecological divergence and convergence, nutritional specificity and plasticity, and allopatric and sympatric speciation. Based on this synthesis, we conclude that the evolutionary pressures shaping these interactions are complex, with influences from both external (nutrient limitation and competition) and internal (fitness trade-offs and evolutionary constraints) factors. We outline recent controversies pertaining to these evolutionary pressures and place our current understanding of these interactions into a broader ecological and evolutionary framework. Finally, we propose areas for future research that we believe will lead to important new developments in the field.

AbstractOn coral reefs, some of the most aggressive calcium carbonate eroders are dinoflagellate-hosting sponges of the genus Cliona. Like in other marine taxa, the influence of these symbiotic microorganisms on the metabolism of the host sponge, and thereby on erosion of the surrounding ecosystem, is increasingly acknowledged. Despite elevating pH (and hence carbonate saturation state), dinoflagellate photosynthesis promotes bioerosion by their hosts. This paradox might be solved by a spatial isolation of photosynthesis from carbonate dissolution, but it remains unknown which mechanism connects the dinoflagellates’ photosynthesis with the sponge’s bioerosion. Here, we simulate the outcomes of photosynthesis in two separate ways, namely as production of carbon-rich compounds (in this case glycerol) and as an increase in oxygen content. This allows testing their potential to enhance bioerosion rates of sponge holobionts that were preconditioned under variable photosynthetic regimes. We find that glycerol, a commonly shared photosynthate in marine symbioses, stimulates chemical bioerosion rates in the dark of photosynthetically impaired sponges. Chemical bioerosion was all the more limited by availability of sufficient oxygen, while the combination of added glycerol and oxygen boosted chemical bioerosion rates. We argue that under normal physiological conditions, bioerosion is promoted by both organic carbon and oxygen production, and we provide evidence for the storage of photosynthates for night-time use. We further discuss our findings in the context of the current knowledge of the bioerosion mechanism, which we expand by integrating the effects of carbon-rich compounds and oxygen as drivers for bioerosion by Cliona.

AbstractAmong the ecological roles that sponges play in marine ecosystems, one of the highlights is their ability to host a wide diversity and abundance of epibenthic organisms. However, of the different marine environments, this role has been less investigated in seagrass-dwelling sponges. In this study, the main objective was to determine whether the structure of the associated faunal assemblages in two common sympatric species of seagrass-dwelling sponges (Amorphinopsis atlantica and Haliclona implexiformis) vary depending on the volume and morphology of the host sponge as well as the environment to which both sponges are exposed. Even though the collection sites had the same habitat type (seagrass meadows composed by Thalassia testudinum and Halodule wrightii) and depth, there were substantial differences in faunal composition (ANOSIM test, R = 0.86) between both sponge species. The value of the data on species richness, diversity, and abundance of associated organisms was significantly higher in the individuals of A. atlantica than in those of H. implexiformis. These differences in the community structure of associated fauna could be influenced by the differential growth form of the hosts (e.g. growth form and oscula diameter) as well as their distinct environmental preferences (sites with different degrees of exposure to wind-generated waves and levels of human disturbance). This study contributes to the knowledge on the functional role that sponges play in seagrass meadows, one of the world’s most endangered ecosystems. Furthermore, it underlines the importance of examining both, the sponge morphology and the local environmental conditions, to explain spatial variations in the macrofaunal assemblages associated with sponges.

Sponges are among the oldest metazoans and their success is partly due to their abundant and diverse microbial symbionts. They are one of the few animals that have Thaumarchaeota symbionts. Here we compare genomes of 11 Thaumarchaeota sponge symbionts, including three new genomes, to free-living ones. Like their free-living counterparts, sponge-associated Thaumarchaeota can oxidize ammonia, fix carbon, and produce several vitamins. Adaptions to life inside the sponge host include enrichment in transposases, toxin-antitoxin systems and restriction modifications systems, enrichments previously reported also from bacterial sponge symbionts. Most thaumarchaeal sponge symbionts lost the ability to synthesize rhamnose, which likely alters their cell surface and allows them to evade digestion by the host. All but one archaeal sponge symbiont encoded a high-affinity, branched-chain amino acid transporter system that was absent from the analyzed free-living thaumarchaeota suggesting a mixotrophic lifestyle for the sponge symbionts. Most of the other unique features found in sponge-associated Thaumarchaeota, were limited to only a few specific symbionts. These features included the presence of exopolyphosphatases and a glycine cleavage system found in the novel genomes. Thaumarchaeota have thus likely highly specific interactions with their sponge host, which is supported by the limited number of host sponge species to which each of these symbionts is restricted.

Interest in bioactive pigments stems from their ecological role in adaptation, as well as their applications in various consumer products. The production of these bioactive pigments can be from a variety of biological sources, including simple microorganisms that may or may not be associated with a host. This study is particularly interested in the marine sponges, which have been known to harbor microorganisms that produce secondary metabolites like bioactive pigments. In this study, marine sponge tissue samples were collected from Puhi Bay off the Eastern shore of Hilo, Hawai‘i and subsequently were identified as Petrosia sp. with red pigmentation. Using surface sterilization and aseptic plating of sponge tissue samples, sponge-associated microorganisms were isolated. One isolate (PPB1) produced a colony with red pigmentation like that of Petrosia sp., suggesting an integral relationship between this particular isolate and the sponge of interest. 16S characterization and sequencing of PPB1 revealed that it belonged to the Pseudoalteromonas genus. Using various biological assays, both antimicrobial and antioxidant bioactivity was shown in Pseudoalteromonas sp. PPB1 crude extract. To further investigate the genetics of pigment production, a draft genome of PPB1 was sequenced, assembled, and annotated. This revealed a prodiginine biosynthetic pathway and the first cited-incidence of a prodiginine-producing Pseudoalteromonas species isolated from a marine sponge host. Further understanding into the bioactivity and biosynthesis of secondary metabolites like pigmented prodiginine may uncover the complex ecological interactions between host sponge and microorganism.

AbstractThe potential of sponge-associated bacteria for the biosynthesis of natural products with antibacterial activity was evaluated. In a preliminary screening 108 of 835 axenic isolates showed antibacterial activity. Active isolates were identified by 16S rRNA gene sequencing and selection of the most promising strains was done in a championship like approach, which can be done in every lab and field station without expensive equipment. In a competition assay, strains that inhibited most of the other strains were selected. In a second round, the strongest competitors from each host sponge competed against each other. To rule out that the best competitors selected in that way represent similar strains with the same metabolic profile, BOX PCR experiments were performed, and extracts of these strains were analysed using metabolic fingerprinting. This proved that the strains are different and have various metabolic profiles, even though belonging to the same genus, i.e. Bacillus. Furthermore, it was shown that co-culture experiments triggered the production of compounds with antibiotic activity, i.e. surfactins and macrolactin A. Since many members of the genus Bacillus possess the genetic equipment for the biosynthesis of these compounds, a potential synergism was analysed, showing synergistic effects between C14-surfactin and macrolactin A against methicillin-resistant Staphylococcus aureus (MRSA).

AbstractProkaryotic associations with sponges are among the oldest host-microbiome relationships on Earth. In this study, we investigated how bacteria from several phyla have independently adapted to the sponge interior by comparing metagenome-assembled genomes of sponge-dwelling and pelagic bacteria sourced from broad phylogenetic and geographic samplings. We discovered that sponge-dwelling bacteria have more energetically expensive genomes and share patterns of depletion and enrichment for functional categories of genes that evidence evolution towards lower pathogenicity. We also identified a new defining genomic characteristic of sponge-dwelling bacteria that is virtually absent from pelagic bacteria, the presence of cassettes that contain eukaryotic steroid biosynthesis genes. Collectively, these results illuminate the trends in genome evolution that are associated with a sponge-dwelling life history strategy and have implications for furthering our understanding of how sponge-microbial symbioses have persisted through deep evolutionary time.ImportanceMuch attention has recently been devoted to investigating the evolution of microbes that live in symbiosis with sponge hosts using microbial metagenomic data. However, several biological questions regarding this symbiosis remain unanswered. Two questions that we address here are: 1) what are the long-term consequences of the symbiosis on the evolution of microbial symbiont genome size, protein content, and nucleotide content, and 2) how is the evolution of virulence in sponge-dwelling microbial symbionts, which generally undergo a mixed transmission modes (e.g. horizontal and vertical), related to long-term stability of the symbiosis? By employing the largest comparative metagenomic analysis to date in terms of host sponge species and geographic representation, we address these questions and provide further resolution into the evolutionary processes that are involved in mediating the crosstalk between sponge hosts and their microbial symbionts.

A new species of the often-cryptic genus Polycheria (Crustacea; Amphipoda) was discovered living in a small specimen of the sponge, Homaxinella erecta (Brøndsted, 1924) (Demospongiae, Suberitida, Suberitidae), in Spirits Bay, on the northern tip of the North Island of New Zealand. Polycheria spongoteras sp. nov. is described using integrative techniques (morphologically, molecularly and ecologically), with discussions on the New Zealand records of the genus and related taxa. The host sponge is redescribed and placed in the Spirits Bay context. [Zooban URL: urn:lsid:zoobank.org:act:FB60B77B-6B98-4102-A41F-D980B03204EB] 

ABSTRACTSponges establish tight associations with both micro- and macroorganisms. However, while studies on sponge microbiomes are numerous, nothing is currently known about the microbiomes of sponge-associated polychaetes and their relationships with those of their host sponges. We analyzed the bacterial communities of symbiotic polychaetes (Haplosyllisspp.) and their host sponges (Clathria reinwardti,Amphimedon paraviridis,Neofibularia hartmani, andAaptos suberitoides) to assess the influence of the sponges on the polychaete microbiomes. We identified both eukaryote partners by molecular (16S and COI genes) and morphological features, and we identified their microbial communities by high-throughput sequencing of the 16S rRNA gene (V4 region). We unravel the existence of sixHaplosyllisspecies (five likely undescribed) associated at very high densities with the study sponge species in Nha Trang Bay (central Vietnam). A single polychaete species inhabitedA. paraviridisand was different from the single species that inhabitedA. suberitoides. Conversely, two different polychaete species were found inC. reinwardtiandN. hartmani, depending on the two host locations. Regardless of the host sponge, polychaete microbiomes were species specific, which is a widespread feature in marine invertebrates. More than half of the polychaete bacteria were also found in the host sponge microbiome but at contrasting abundances. Thus, the associated polychaetes seemed to be able to select, incorporate, and enrich part of the sponge microbiome, a selection that appears to be polychaete species specific. Moreover, the bacterial diversity is similar in both eukaryotic partners, which additionally confirms the influence of food (host sponge) on the structure of the polychaete microbiome.IMPORTANCEThe symbiotic lifestyle represents a fundamental cryptic contribution to the diversity of marine ecosystems. Sponges are ideal targets to improve understanding the symbiotic relationships from evolutionary and ecological points of view, because they are the most ancient metazoans on earth, are ubiquitous in the marine benthos, and establish complex symbiosis with both prokaryotes and animals, which in turn also harbor their own bacterial communities. Here, we study the microbiomes of sponge-polychaete associations and confirm that polychaetes feed on their host sponges. The study worms select and enrich part of the sponge microbiome to shape their own species-specific bacterial communities. Moreover, worm microbiome diversity runs parallel to that of its food host sponge. Considering our results on symbiotic polychaetes and previous studies on fishes and mammals, diet appears to be an important source of bacteria for animals to shape their species-specific microbiomes.