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- Comparative metagenomics reveals the distinctive adaptive features of the Spongia officinalis endosymbiotic consortiumPublication . Karimi, Elham; Ramos, Miguel; Gonçalves, Jorge Manuel Santos; Xavier, Joana R.; Reis, Margarida; Costa, RodrigoCurrent knowledge of sponge microbiome functioning derives mostly from comparative analyses with bacterioplankton communities. We employed a metagenomics-centered approach to unveil the distinct features of the Spongia officinalis endosymbiotic consortium in the context of its two primary environmental vicinities. Microbial metagenomic DNA samples (n = 10) from sponges, seawater, and sediments were subjected to Hiseq Illumina sequencing (c. 15 million 100 bp reads per sample). Totals of 10,272 InterPro (IPR) predicted protein entries and 784 rRNA gene operational taxonomic units (OTUs, 97% cut-off) were uncovered from all metagenomes. Despite the large divergence in microbial community assembly between the surveyed biotopes, the S. officinalis symbiotic community shared slightly greater similarity (p < 0.05), in terms of both taxonomy and function, to sediment than to seawater communities. The vast majority of the dominant S. officinalis symbionts (i.e., OTUs), representing several, so-far uncultivable lineages in diverse bacterial phyla, displayed higher residual abundances in sediments than in seawater. CRISPR-Cas proteins and restriction endonucleases presented much higher frequencies (accompanied by lower viral abundances) in sponges than in the environment. However, several genomic features sharply enriched in the sponge specimens, including eukaryotic-like repeat motifs (ankyrins, tetratricopeptides, WD-40, and leucine-rich repeats), and genes encoding for plasmids, sulfatases, polyketide synthases, type IV secretion proteins, and terpene/terpenoid synthases presented, to varying degrees, higher frequencies in sediments than in seawater. In contrast, much higher abundances of motility and chemotaxis genes were found in sediments and seawater than in sponges. Higher cell and surface densities, sponge cell shedding and particle uptake, and putative chemical signaling processes favoring symbiont persistence in particulate matrices all may act as mechanisms underlying the observed degrees of taxonomic connectivity and functional convergence between sponges and sediments. The reduced frequency of motility and chemotaxis genes in the sponge microbiome reinforces the notion of a prevalent mutualistic mode of living inside the host. This study highlights the S. officinalis "endosymbiome" as a distinct consortium of uncultured prokaryotes displaying a likely "sit-and-wait" strategy to nutrient foraging coupled to sophisticated anti-viral defenses, unique natural product biosynthesis, nutrient utilization and detoxification capacities, and both microbe-microbe and host-microbe gene transfer amenability.
- Molecular richness and biotechnological potential of bacteria cultured from Irciniidae sponges in the north-east AtlanticPublication . Esteves, Ana; Hardoim, Cristiane; Xavier, Joana R.; Gonçalves, Jorge Manuel Santos; Costa, RodrigoSeveral bioactive compounds originally isolated from marine sponges have been later ascribed or suggested to be synthesized by their symbionts. The cultivation of sponge-associated bacteria provides one possible route to the discovery of these metabolites. Here, we determine the bacterial richness cultured from two irciniid sponge species, Sarcotragus spinosulus and Ircinia variabilis, and ascertain their biotechnological potential. A total of 279 isolates were identified from 13 sponge specimens. These were classified into 17 genera - with Pseudovibrio, Ruegeria and Vibrio as the most dominant - and 3 to 10 putatively new bacterial species. While 16S rRNA gene sequencing identified 29 bacterial phylotypes at the 'species' level (97% sequence similarity), whole-genome BOX-PCR fingerprinting uncovered 155 genotypes, unveiling patterns of specimen-dependent occurrence of prevailing bacterial genomes across sponge individuals. Among the BOX-PCR genotypes recovered, 34% were active against clinically relevant strains, with Vibrio isolates producing the most active antagonistic effect. Several Pseudovibrio genotypes showed the presence of polyketide synthase (PKS) genes, and these were for the first time detected in isolates of the genus Aquimarina (Bacteroidetes). Our results highlight great biotechnological potential and interest for the Irciniidae sponge family and their diversified bacterial genomes.
- Functional metagenomics reveals differential chitin degradation and utilization features across free-living and host-associated marine microbiomesPublication . Raimundo, I.; Silva, R.; Meunier, L.; Valente, S. M.; Lago-Lestón, A.; Keller-Costa, T.; Costa, RodrigoBackground Chitin ranks as the most abundant polysaccharide in the oceans yet knowledge of shifts in structure and diversity of chitin-degrading communities across marine niches is scarce. Here, we integrate cultivation-dependent and -independent approaches to shed light on the chitin processing potential within the microbiomes of marine sponges, octocorals, sediments, and seawater. Results We found that cultivatable host-associated bacteria in the genera Aquimarina, Enterovibrio, Microbulbifer, Pseudoalteromonas, Shewanella, and Vibrio were able to degrade colloidal chitin in vitro. Congruent with enzymatic activity bioassays, genome-wide inspection of cultivated symbionts revealed that Vibrio and Aquimarina species, particularly, possess several endo- and exo-chitinase-encoding genes underlying their ability to cleave the large chitin polymer into oligomers and dimers. Conversely, Alphaproteobacteria species were found to specialize in the utilization of the chitin monomer N-acetylglucosamine more often. Phylogenetic assessments uncovered a high degree of within-genome diversification of multiple, full-length endo-chitinase genes for Aquimarina and Vibrio strains, suggestive of a versatile chitin catabolism aptitude. We then analyzed the abundance distributions of chitin metabolism-related genes across 30 Illumina-sequenced microbial metagenomes and found that the endosymbiotic consortium of Spongia officinalis is enriched in polysaccharide deacetylases, suggesting the ability of the marine sponge microbiome to convert chitin into its deacetylated—and biotechnologically versatile—form chitosan. Instead, the abundance of endo-chitinase and chitin-binding protein-encoding genes in healthy octocorals leveled up with those from the surrounding environment but was found to be depleted in necrotic octocoral tissue. Using cultivation-independent, taxonomic assignments of endo-chitinase encoding genes, we unveiled previously unsuspected richness and divergent structures of chitinolytic communities across host-associated and free-living biotopes, revealing putative roles for uncultivated Gammaproteobacteria and Chloroflexi symbionts in chitin processing within sessile marine invertebrates. Conclusions Our findings suggest that differential chitin degradation pathways, utilization, and turnover dictate the processing of chitin across marine micro-niches and support the hypothesis that inter-species cross-feeding could facilitate the co-existence of chitin utilizers within marine invertebrate microbiomes. We further identified chitin metabolism functions which may serve as indicators of microbiome integrity/dysbiosis in corals and reveal putative novel chitinolytic enzymes in the genus Aquimarina that may find applications in the blue biotechnology sector. Video abstract
- Diversity of the candidate phylum Poribacteria in the marine sponge Aplysina fulvaPublication . Hardoim, Cristiane; Cox, C. J.; Peixoto, R. S.; Rosado, A. S.; da Silva Costa, Rodrigo; Van Elsas, J. D.Poribacterial clone libraries constructed for Aplysina fulva sponge specimens were analysed with respect to diversity and phylogeny. Results imply the coexistence of several, prevalently “intraspecific” poribacterial genotypes in a single sponge host, and suggest quantitative analysis as a desirable approach in studies of the diversity and distribution of poribacterial cohorts in marine sponges.