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Candidatus Nemesobacterales is a sponge-specific clade of the candidate phylum Desulfobacterota adapted to a symbiotic lifestyle

The ISME Journal volume 17, pages 1808–1818 (2023)Cite this article

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Abstract

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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Fig. 1: Phylogenomic tree of Ca. Dadabacteria (GTDB-Desulfobacterota__D) based on the concatenated alignment of 120 bacterial single-copy marker protein sequences (5 037 positions).
Fig. 2: Schematic map representing the global distribution of Ca. Nemesobacterales.
Fig. 3: Schematic overview of the inferred metabolism of Ca. Nemesobacterales.
Fig. 4: Functional comparison of Ca. Dadabacteria (GTDB-Desulfobacterota__D) MAGs associated with marine sponges and seawater.
Fig. 5: Imaging of Ca. Nemesobacterales spp. in G. barretti.

Data availability

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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Acknowledgements

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.

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Authors and Affiliations

  1. Laboratory of Microbiology, Wageningen University & Research, Stippeneng 4, 6708WE, Wageningen, The Netherlands

    Asimenia Gavriilidou, Burak Avcı, Anastasia Galani, Michelle A. Schorn, Thijs J. G. Ettema, Hauke Smidt & Detmer Sipkema

  2. Hoekmine BV, Verenigingstraat 36, 3515GJ, Utrecht, The Netherlands

    Colin J. Ingham

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Contributions

AsG, CJI, HS and DS conceived the study. AsG, AnG and DS collected the sponge samples. AsG, AnG and MAS processed the samples for sequencing. AnG and MAS did the quality filtering of raw reads, metagenome assemblies, binning and taxonomic classification (Aply, DOM and PF samples). AsG performed the binning and taxonomic classification of the GA and GB samples. AsG performed the MAG collection, phylogenetic analysis, metabolic reconstruction, comparative genomic analysis, statistical analysis and visualization. BA performed the oligonucleotide probe design, FISH and microscopy. All authors contributed to the interpretation of the results. AsG wrote the first draft and all authors edited and approved the manuscript.

Corresponding authors

Correspondence to Asimenia Gavriilidou or Detmer Sipkema.

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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

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