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ABSTRACT Members of the widespread bacterial phylum Chloroflexi can dominate high-microbial-abundance (HMA) sponge microbiomes. In the Sponge Microbiome Project, Chloroflexi sequences amounted to 20 to 30% of the total microbiome of certain HMA sponge genera with the classes/clades SAR202, Caldilineae, and An- aerolineae being the most prominent. We performed metagenomic and single- cell genomic analyses to elucidate the functional gene repertoire of Chloroflexi symbionts of Aplysina aerophoba. Eighteen draft genomes were reconstructed and placed into phylogenetic context of which six were investigated in detail. Common genomic features of Chloroflexi sponge symbionts were related to central energy and carbon converting pathways, amino acid and fatty acid metabolism, and respiration. Clade-specific metabolic features included a massively expanded genomic repertoire for carbohydrate degradation in Anaerolineae and Caldilineae ge- nomes, but only amino acid utilization by SAR202. While Anaerolineae and Caldilin- eae import cofactors and vitamins, SAR202 genomes harbor genes encoding compo- nents involved in cofactor biosynthesis. A number of features relevant to symbiosis were further identified, including CRISPR-Cas systems, eukaryote-like repeat proteins, and secondary metabolite gene clusters. Chloroflexi symbionts were visualized in the sponge extracellular matrix at ultrastructural resolution by the fluorescence in situ hybridization-correlative light and electron microscopy (FISH-CLEM) method. Carbo- hydrate degradation potential was reported previously for "Candidatus Poribacteria" and SAUL, typical symbionts of HMA sponges, and we propose here that HMA sponge symbionts collectively engage in degradation of dissolved organic matter, both labile and recalcitrant. Thus, sponge microbes may not only provide nutrients to the sponge host, but they may also contribute to dissolved organic matter (DOM) recycling and primary productivity in reef ecosystems via a pathway termed the sponge loop. I M P O R T A N C E ...

11 pages, 5 figures, 1 table, supplementary information https://doi.org/10.1038/s41396-021-00900-6 ; Bacteriophages (phages) are ubiquitous elements in nature, but their ecology and role in animals remains little understood. Sponges represent the oldest known extant animal-microbe symbiosis and are associated with dense and diverse microbial consortia. Here we investigate the tripartite interaction between phages, bacterial symbionts, and the sponge host. We combined imaging and bioinformatics to tackle important questions on who the phage hosts are and what the replication mode and spatial distribution within the animal is. This approach led to the discovery of distinct phage-microbe infection networks in sponge versus seawater microbiomes. A new correlative in situ imaging approach ('PhageFISH-CLEM') localised phages within bacterial symbiont cells, but also within phagocytotically active sponge cells. We postulate that the phagocytosis of free virions by sponge cells modulates phage-bacteria ratios and ultimately controls infection dynamics. Prediction of phage replication strategies indicated a distinct pattern, where lysogeny dominates the sponge microbiome, likely fostered by sponge host-mediated virion clearance, while lysis dominates in seawater. Collectively, this work provides new insights into phage ecology within sponges, highlighting the importance of tripartite animal-phage-bacterium interplay in holobiont functioning. We anticipate that our imaging approach will be instrumental to further understanding of viral distribution and cellular association in animal hosts ; We acknowledge funding by the DFG CRC1182 to UH (TPC4.3), TL (TPC4.2). MTJ was supported by a grant of the German Excellence Initiative to the Graduate School of Life Sciences, University of Wuerzburg, and a Young Investigator Award of the CRC1182. SMM was supported by the Studienstiftung des Deutschen Volkes (German Academic Scholarship Foundation). CS was supported by the grants DFG STI700/1-1 and GRK2581 (P6). MR was supported by the Spanish Government grant (RTI2018-094187-B100) and 'Generalitat de Catalunya' research group grant (2017SGR1011). BED was supported by the Netherlands Organisation for Scientific Research (NWO) Vidi grant 864.14.004 and by the European Research Council (ERC) Consolidator grant 865694: DiversiPHI. /./ Open Access funding enabled and organized by Projekt DEA ; With the funding support of the 'Severo Ochoa Centre of Excellence' accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI) ; Peer reviewed

Estee artículo contiene 14 páginas, 6 figuras. ; Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean. ; This work was funded by the DFG CRC1182-TP B1 "Origin and Function of Metaorganisms" to UH, the Spanish Government grant (RTI2018–094187-B100) and "Generalitat de Catalunya" research group grant (2017SGR1011) to MR and RC, the Netherlands Organization for Scientific Research (NWO-VIDI 864.13.007) to DvO, the European Research Council under the European Union's Horizon 2020 research and innovation programme (Starting Grant 715513) to JMG, and the Swiss Science Foundation Grant (200021_179092) to AM. ; Peer reviewed