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Members of the candidate phylum Dadabacteria, recently reassigned to the phylum Candidatus Desulfobacterota, are cosmopolitan in the marine environment, and are found both free-living and associated with hosts that are mainly marine sponges. Yet, these microorganisms are poorly characterised, showing an ambiguous phylogeny and having no cultured representatives. Here, we performed genome-centric metagenomics to elucidate the phylogeny and predict the metabolism of the sponge-associated members of this lineage. Rank-based phylogenomics revealed several new species and a novel family (Candidatus Spongomicrobiaceae) within a sponge-specific order, named here Candidatus Nemesobacterales (GTDB order RKRQ01). Metabolic reconstruction suggests that Ca. Nemesobacterales are aerobic heterotrophs, capable of synthesizing most amino acids, vitamins and cofactors and degrading complex carbohydrates. We also report functional divergence between sponge- and seawater-associated metagenome-assembled genomes (MAGs). Niche-specific adaptations to the sponge holobiont were evident from significantly enriched genes involved in defense mechanisms against foreign DNA and environmental stressors, host-symbiont interactions and secondary metabolite production. Fluorescencet in situ hybridization (FISH) gave a first glimpse of the morphology and lifestyle of a member of Ca. Desulfobacterota. The Candidatus Nemesobacterales spp. rappii wereas found inside bacteriocytes in the tissue mesohyl of the sponge Geodia barretti. Altogether, this is the first study that sheds light on the enigmatic group Ca. Nemesobacterales and their functional characteristics which reflect a symbiotic lifestyle., Members of the candidate phylum Dadabacteria, recently reassigned to the phylum Candidatus Desulfobacterota, are cosmopolitan in the marine environment, and are found both free-living and associated with hosts that are mainly marine sponges. Yet, these microorganisms are poorly characterised, showing an ambiguous phylogeny and having no cultured representatives. Here, we performed genome-centric metagenomics to elucidate the phylogeny and predict the metabolism of the sponge-associated members of this lineage. Rank-based phylogenomics revealed several new species and a novel family (Candidatus Spongomicrobiaceae) within a sponge-specific order, named here Candidatus Nemesobacterales (GTDB order RKRQ01). Metabolic reconstruction suggests that Ca. Nemesobacterales are aerobic heterotrophs, capable of synthesizing most amino acids, vitamins and cofactors and degrading complex carbohydrates. We also report functional divergence between sponge- and seawater-associated metagenome-assembled genomes (MAGs). Niche-specific adaptations to the sponge holobiont were evident from significantly enriched genes involved in defense mechanisms against foreign DNA and environmental stressors, host-symbiont interactions and secondary metabolite production. Fluorescencet in situ hybridization (FISH) gave a first glimpse of the morphology and lifestyle of a member of Ca. Desulfobacterota. The Candidatus Nemesobacterales spp. rappii wereas found inside bacteriocytes in the tissue mesohyl of the sponge Geodia barretti. Altogether, this is the first study that sheds light on the enigmatic group Ca. Nemesobacterales and their functional characteristics which reflect a symbiotic lifestyle.

Genomic and functional analyses of bacteria belonging to the candidate genus ‘Entotheonella’ have revealed them as the producers of diverse bioactive compounds previously identified from their sponge hosts. Based on genetic distance to other taxa, ‘Candidatus Entotheonella’ has been proposed as the first member of a new candidate phylum, ‘Tectomicrobia’. Here, we analysed environmental samples and publicly available 16S ribosomal RNA (rRNA) gene sequences to assess the phylogenetic structure and environmental distribution of this as-yet sparsely populated lineage. The data showed that ‘Ca. Entotheonella’ and other 'Ca. Tectomicrobia' were not restricted to marine habitats but also widely distributed among terrestrial locations. Environmental factors, such as water depth and host association were identified to correlate with the phylogenetic patterns of marine phylotypes. The previously described ‘Ca. Entotheonella’ lineage could be more accurately divided into at least three different candidate genera with the terrestrial 'Candidatus Prasianella', the marine 'Candidatus Thalassonella' and the more widely distributed 'Ca. Entotheonella' of mixed origin. This first metagenomic and microscopic characterization of 'Ca. Thalassonella' from a range of sponge hosts did not suggest a role for its members as providers of natural products, despite clear similarities in genome-based predictions of primary metabolism and implied lifestyle with ‘Ca. Entotheonella’. In contrast, within the revised ‘Ca. Entotheonella’, the analysis revealed a correlation between the 16S rRNA gene phylogeny and a specific association with sponges and their chemistry, suggesting that this feature might serve as a discovery method to accelerate the identification of new ‘Ca. Entotheonella’ producers of bioactive compounds. Application of this strategy led to the identification of the first ‘Ca. Entotheonella’ symbiont in a non-lithistid sponge, Psammocinia sp., thus indicating a wider host distributi, Genomic and functional analyses of bacteria belonging to the candidate genus ‘Entotheonella’ have revealed them as the producers of diverse bioactive compounds previously identified from their sponge hosts. Based on genetic distance to other taxa, ‘Candidatus Entotheonella’ has been proposed as the first member of a new candidate phylum, ‘Tectomicrobia’. Here, we analysed environmental samples and publicly available 16S ribosomal RNA (rRNA) gene sequences to assess the phylogenetic structure and environmental distribution of this as-yet sparsely populated lineage. The data showed that ‘Ca. Entotheonella’ and other 'Ca. Tectomicrobia' were not restricted to marine habitats but also widely distributed among terrestrial locations. Environmental factors, such as water depth and host association were identified to correlate with the phylogenetic patterns of marine phylotypes. The previously described ‘Ca. Entotheonella’ lineage could be more accurately divided into at least three different candidate genera with the terrestrial 'Candidatus Prasianella', the marine 'Candidatus Thalassonella' and the more widely distributed 'Ca. Entotheonella' of mixed origin. This first metagenomic and microscopic characterization of 'Ca. Thalassonella' from a range of sponge hosts did not suggest a role for its members as providers of natural products, despite clear similarities in genome-based predictions of primary metabolism and implied lifestyle with ‘Ca. Entotheonella’. In contrast, within the revised ‘Ca. Entotheonella’, the analysis revealed a correlation between the 16S rRNA gene phylogeny and a specific association with sponges and their chemistry, suggesting that this feature might serve as a discovery method to accelerate the identification of new ‘Ca. Entotheonella’ producers of bioactive compounds. Application of this strategy led to the identification of the first ‘Ca. Entotheonella’ symbiont in a non-lithistid sponge, Psammocinia sp., thus indicating a wider host distributi

Genomic and functional analyses of bacterial sponge symbionts belonging to the uncultivated candidate genus ‘Entotheonella’ has revealed them as the prolific producers of bioactive compounds previously identified from their invertebrate hosts. These studies also suggested ‘Entotheonella’ as the first members of a new candidate phylum, ‘Tectomicrobia’. Here we analyzed the phylogenetic structure and environmental distribution of this as-yet sparsely populated phylum-like lineage. The data show that ‘Entotheonella’ and other ‘Tectomicrobia’ are not restricted to marine habitats but widely distributed among terrestrial locations. The inferred phylogenetic trees suggest several intra-phylum lineages with diverse lifestyles. Of these, the previously described ‘Entotheonella’ lineage can be more accurately divided into at least three different candidate genera with the terrestrial ‘Candidatus Prasianella’, the largely terrestrial ‘Candidatus Allonella’, the ‘Candidatus Thalassonella’ comprising sponge-associated members, and the more widely distributed ‘Candidatus Entotheonella’. Genomic characterization of ‘Thalassonella’ members from a range of sponge hosts did not suggest a role as providers of natural products, despite high genomic similarity to ‘Entotheonella’ regarding primary metabolism and implied lifestyle. In contrast, the analysis revealed a correlation between the revised ‘Entotheonella’ 16S rRNA gene phylogeny and a specific association with sponges and their natural products. This feature might serve as a discovery method to accelerate the identification of new chemically rich ‘Entotheonella’ variants, and led to the identification of the first ‘Entotheonella’ symbiont in a non-tetractinellid sponge, Psammocinia sp., indicating a wide host distribution of ‘Entotheonella’-based chemical symbiosis.

Genomic and functional analyses of bacterial sponge symbionts belonging to the uncultivated candidate genus ‘Entotheonella’ has revealed them as the prolific producers of bioactive compounds previously identified from their invertebrate hosts. These studies also suggested ‘Entotheonella’ as the first members of a new candidate phylum, ‘Tectomicrobia’. Here we analyzed the phylogenetic structure and environmental distribution of this as-yet sparsely populated phylum-like lineage. The data show that ‘Entotheonella’ and other ‘Tectomicrobia’ are not restricted to marine habitats but widely distributed among terrestrial locations. The inferred phylogenetic trees suggest several intra-phylum lineages with diverse lifestyles. Of these, the previously described ‘Entotheonella’ lineage can be more accurately divided into at least three different candidate genera with the terrestrial ‘Candidatus Prasianella’, the largely terrestrial ‘Candidatus Allonella’, the ‘Candidatus Thalassonella’ comprising sponge-associated members, and the more widely distributed ‘Candidatus Entotheonella’. Genomic characterization of ‘Thalassonella’ members from a range of sponge hosts did not suggest a role as providers of natural products, despite high genomic similarity to ‘Entotheonella’ regarding primary metabolism and implied lifestyle. In contrast, the analysis revealed a correlation between the revised ‘Entotheonella’ 16S rRNA gene phylogeny and a specific association with sponges and their natural products. This feature might serve as a discovery method to accelerate the identification of new chemically rich ‘Entotheonella’ variants, and led to the identification of the first ‘Entotheonella’ symbiont in a non-tetractinellid sponge, Psammocinia sp., indicating a wide host distribution of ‘Entotheonella’-based chemical symbiosis.

Marine sponges represent an excellent example of host-microbe symbiosis. Yet, most sponge-associated microorganisms remain uncultured, hampering efforts in determining interactions with their sponge host. This project aimed at enhancing our understanding of the sponge-bacteria interplay, focusing on both cultured and yet-uncultured sponge-associated lineages. Several novel sponge-associated taxa were elucidated by resolving their phylogeny and reconstructing their primary and secondary metabolism. Genome-based predictions revealed that the sponge microbiome mediates the interactions of the holobiont via heterotrophy, potential metabolite exchange and chemical defense. Sponge symbionts also possessed an extended genomic repertoire of defense systems implying adaptation to host environment. Moreover, genome mining for biosynthetic gene clusters (BGCs) and bioactivity screening of sponge-associated strains detected many candidate BGCs potentially involved in observed anticancer and antibacterial activity. Altogether, this work shed light into novel sponge-associated phylotypes, features that point at a symbiotic lifestyle and a rich secondary metabolite biosynthesis arsenal with biotechnological potential.

In the deep ocean symbioses between microbes and invertebrates are emerging as key drivers of ecosystem health and services. We present a large-scale analysis of microbial diversity in deep-sea sponges (Porifera) from scales of sponge individuals to ocean basins, covering 52 locations, 1077 host individuals translating into 169 sponge species (including understudied glass sponges), and 469 reference samples, collected anew during 21 ship-based expeditions. We demonstrate the impacts of the sponge microbial abundance status, geographic distance, sponge phylogeny, and the physicalbiogeochemical environment as drivers of microbiome composition, in descending order of relevance. Our study further discloses that fundamental concepts of sponge microbiology apply robustly to sponges from the deep-sea across distances of >10,000 km. Deep-sea sponge microbiomes are less complex, yet more heterogeneous, than their shallow-water counterparts. Our analysis underscores the uniqueness of each deep-sea sponge ground based on which we provide critical knowledge for conservation of these vulnerable ecosystems.

Marine sponges and their microbial symbiotic communities are rich sources of diverse natural products (NPs) that often display biological activity, yet little is known about the global distribution of NPs and the symbionts that produce them. Since the majority of sponge symbionts remain uncultured, it is a challenge to characterize their NP biosynthetic pathways, assess their prevalence within the holobiont, and measure the diversity of NP biosynthetic gene clusters (BGCs) across sponge taxa and environments. Here, we explore the microbial biosynthetic landscapes of three high-microbial-abundance (HMA) sponges from the Atlantic Ocean and the Mediterranean Sea. This data set reveals striking novelty, with,1% of the recovered gene cluster families (GCFs) showing similarity to any characterized BGC. When zooming in on the microbial communities of each sponge, we observed higher variability of specialized metabolic and taxonomic profiles between sponge species than within species. Nonetheless, we identified conservation of GCFs, with 20% of sponge GCFs being shared between at least two sponge species and a GCF core comprised of 6% of GCFs shared across all species. Within this functional core, we identified a set of widespread and diverse GCFs encoding nonribosomal peptide synthetases that are potentially involved in the production of diversified ether lipids, as well as GCFs putatively encoding the production of highly modified proteusins. The present work contributes to the small, yet growing body of data characterizing NP landscapes of marine sponge symbionts and to the cryptic biosynthetic potential contained in this environmental niche.

specialised metabolism characterisation of metagenomes of three high microbial abundance marine sponges, aplysina aerophoba, petrosia ficiformis and geodia barretti. assemblies and binned genomes were generated and analysed for presence and diversity of biosynthetic gene clusters., specialised metabolism characterisation of metagenomes of three high microbial abundance marine sponges, aplysina aerophoba, petrosia ficiformis and geodia barretti. assemblies and binned genomes were generated and analysed for presence and diversity of biosynthetic gene clusters.

This dataset includes raw sequencing reads, draft genome assemblies and 16S rRNA gene sequences of bacteria isolated from different marine sponge species.

Marine sponges harbor diverse microbial communities that represent a significant source of natural products. In the present study, extracts of 21 sponge-associated bacteria were screened for their antimicrobial and anticancer activity, and their genomes were mined for secondary metabolite biosynthetic gene clusters (BGCs). Phylogenetic analysis assigned the strains to four major phyla in the sponge microbiome, namely Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes. Bioassays identified one extract with anti-methicillin-resistant Staphylococcus aureus (MRSA) activity, and more than 70% of the total extracts had a moderate to high cytotoxicity. The most active extracts were derived from the Proteobacteria and Actinobacteria, prominent for producing bioactive substances. The strong bioactivity potential of the aforementioned strains was also evident in the abundance of BGCs, which encoded mainly beta-lactones, bacteriocins, non-ribosomal peptide synthetases (NRPS), terpenes, and siderophores. Gene-trait matching was performed for the most active strains, aiming at linking their biosynthetic potential with the experimental results. Genetic associations were established for the anti-MRSA and cytotoxic phenotypes based on the similarity of the detected BGCs with BGCs encoding natural products with known bioactivity. Overall, our study highlights the significance of combining in vitro and in silico approaches in the search of novel natural products of pharmaceutical interest.

Genomic sequences of sponge-derived Flavobacteriaceae were generated. A comparative genomics analysis elucidated the functional repertoire of the family Flavobacteriaceae from different environmental sources, with a focus on the Marine clade.