Members of the candidate phylum Dadabacteria, recently reassigned to the phylum Candidatus Desulfobacterota, are cosmopolitan in the marine environment found both free-living and associated with hosts that are mainly marine sponges. Yet, these microorganisms are poorly characterized, with no cultured representatives and an ambiguous phylogenetic position in the tree of life. Here, we performed genome-centric metagenomics to elucidate their phylogenomic placement 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. 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. 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. Fluorescence in situ hybridization gave a first glimpse of the morphology and lifestyle of a member of Ca. Desulfobacterota. Candidatus Nemesobacterales spp. were found both inside sponge cells centred around sponge nuclei and in the mesohyl of the sponge Geodia barretti. This study sheds light on the enigmatic group Ca. Nemesobacterales and their functional characteristics that reflect a symbiotic lifestyle.
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Raw reads, metagenome assemblies and MAGs generated for this study can be found under the European Nucleotide Archive (ENA) project accession numbers PRJEB54590, PRJEB51534 and PRJEB51535. All accession numbers for the data included in this study are included in the supplementary information of this article.
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The authors would like to thank the late Hans Tore Rapp for his invaluable help in collecting G. barretti samples from Norway, Ellen Kenchington for the Canadian G. barretti samples, Vasilis Gerovasileiou for performing the sampling of P. ficiformis and Andriaan Schrier for supporting the sponge collection in Dominica. Henk Schipper is acknowledged for helping with the sponge tissue processing. The authors would like to thank Catarina Loureiro for performing the preprocessing of the reads, the metagenome assembly and binning of the A. aerophoba samples and for her feedback regarding the manuscript. We thank Paco Cárdenas and Karin Steffen for the identification of G. atlantica. We also thank Torsten Thomas for providing us with additional data for our analysis. Maria Chuvochina, Donovan Parks and Philip Hugenholtz are acknowledged for their advice on taxonomy and rank assignment. This research was financially supported by the European Commission through the SponGES project (Grant agreement ID: 679849) to DS and AsG, a Marie Skłodowska-Curie Individual Fellowship COSMos (Grant agreement ID: 897121) to MAS, and by grants from European Research Council (ERC consolidator grant 817834), the Dutch Research Council (NWO-VICI grant VI.C.192.016), and the Moore–Simons Project on the Origin of the Eukaryotic Cell (Simons Foundation 735925LPI) to TJGE.
The authors declare no competing interests.
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Gavriilidou, A., Avcı, B., Galani, A. et al. Candidatus Nemesobacterales is a sponge-specific clade of the candidate phylum Desulfobacterota adapted to a symbiotic lifestyle. ISME J 17, 1808–1818 (2023). https://doi.org/10.1038/s41396-023-01484-z