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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.
- Genomic blueprints of sponge-prokaryote symbiosis are shared by low abundant and cultivatable AlphaproteobacteriaPublication . Karimi, Elham; Keller-Costa, Tina; Slaby, Beate M; Cox, Cymon; da Rocha, Ulisses N; Hentschel, Ute; da Silva Costa, RodrigoMarine sponges are early-branching, filter-feeding metazoans that usually host complex microbiomes comprised of several, currently uncultivatable symbiotic lineages. Here, we use a low-carbon based strategy to cultivate low-abundance bacteria from Spongia officinalis. This approach favoured the growth of Alphaproteobacteria strains in the genera Anderseniella, Erythrobacter, Labrenzia, Loktanella, Ruegeria, Sphingorhabdus, Tateyamaria and Pseudovibrio, besides two likely new genera in the Rhodobacteraceae family. Mapping of complete genomes against the metagenomes of S. officinalis, seawater, and sediments confirmed the rare status of all the above-mentioned lineages in the marine realm. Remarkably, this community of low-abundance Alphaproteobacteria possesses several genomic attributes common to dominant, presently uncultivatable sponge symbionts, potentially contributing to host fitness through detoxification mechanisms (e.g. heavy metal and metabolic waste removal, degradation of aromatic compounds), provision of essential vitamins (e.g. B6 and B12 biosynthesis), nutritional exchange (especially regarding the processing of organic sulphur and nitrogen) and chemical defence (e.g. polyketide and terpenoid biosynthesis). None of the studied taxa displayed signs of genome reduction, indicative of obligate mutualism. Instead, versatile nutrient metabolisms along with motility, chemotaxis, and tight-adherence capacities - also known to confer environmental hardiness - were inferred, underlying dual host-associated and free-living life strategies adopted by these diverse sponge-associated Alphaproteobacteria.
- Metagenomics and functional genomics of bacterial symbionts of Spongia (Porifera, Dictyoceratida) specimens from the Algarvian shore (South Portugal)Publication . Karimi, Elham; Reis, Margarida P.; Costa, Rodrigo da SilvaSponges are early-branched, filter-feeding metazoans that usually harbor complex microbial communities comprised of diverse “uncultivable” symbiotic bacteria. In this thesis, the functional and taxonomic features of the marine sponge microbiome are determined, using Spongia officinalis as model host organism. Emphasis is given to adaptive and functional traits of the profuse and biotechnologically-relevant alphaproteobacterial symbionts of sponges. A metagenomics-centred approach was employed to reveal microbial taxa and genomic signatures enriched in the Spongia officinalis endosymbiotic consortium, and thus likely to play pivotal roles in holobiont functioning. Further, a comparative genomics study is presented unveiling the common and specific traits of ten Alphaproteobacteria genera isolated from S. officinalis with alternative symbiont cultivation methodology. Finally, a sequence composition-dependent binning approach is employed to assemble, from metagenomic sequences, the genome of an uncultured alphaproteobacterial symbiont of S. officinalis belonging to the family Rhodospirillaceae. High abundance of polyketide and terpene synthase-, eukaryotic-like protein- (ELPs), type IV secretion system-, plasmid- and ABC transporter-encoding genes, among others, characterized the sponge microbial metagenomes. In contrast, motility and chemotaxis genes were abundant in seawater and sediment microbiomes, but nearly absent in the S. officinalis symbiotic consortium. Much higher frequencies of anti-viral CRISPR-Cas and restrictionmodification systems, along with much lower viral abundances, were observed in the spongeassociated metagenomes than in the environment and interpreted as true hallmarks of this symbiotic consortium. In line with outcomes retrieved for the whole symbiotic community, alphaproteobacterial symbionts of marine sponges likely contribute the most to host fitness through nutritional exchange, cell detoxification processes and chemical defense, the latter being theoretically promoted by both polyketide and terpenoid biosynthesis. The several alphaproteobacterial cultures retrieved in this thesis, displaying high natural product biosynthesis capacities, can now be explored in studies aiming at revealing novel biological activities and chemical structures from these symbionts.