Phylogeny resolved, metabolism revealed: functional radiation within a widespread and divergent clade of sponge symbionts

Abstract

The symbiosis between bacteria and sponges has arguably the longest evolutionary history for any extant metazoan lineage, yet little is known about bacterial evolution or adaptation in this process. An example of often dominant and widespread bacterial symbionts of sponges is a clade of uncultured and uncharacterised Proteobacteria. Here we set out to characterise this group using metagenomics, in-depth phylogenetic analyses, metatranscriptomics, and fluorescence in situ hybridisation microscopy. We obtained five metagenome-assembled-genomes (MAGs) from different sponge species that, together with a previously published MAG (AqS2), comprise two families within a new gammaproteobacterial order that we named UTethybacterales. Members of this order share a heterotrophic lifestyle but vary in their predicted ability to use various carbon, nitrogen and sulfur sources, including taurine, spermidine and dimethylsulfoniopropionate. The deep branching of the UTethybacterales within the Gammaproteobacteria and their almost exclusive presence in sponges suggests they have entered a symbiosis with their host relatively early in evolutionary time and have subsequently functionally radiated. This is reflected in quite distinct lifestyles of various species of UTethybacterales, most notably their diverse morphologies, predicted substrate preferences, and localisation within the sponge tissue. This study provides new insight into the evolution of metazoan–bacteria symbiosis.

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Fig. 1: 16S rRNA phylogenetic tree of gammaproteobacterial orders with Alphaproteobacteria as an outgroup.
Fig. 2: Phylogenomic tree of the Proteobacteria based on GTDB.
Fig. 3: Global distribution of UTethybacterales-containing samples collected for the Sponge Earth Microbiome Project.
Fig. 4: Detection of UTethybacterales species by CARD-FISH in sponge hosts.

Data availability

Raw sequencing data are publicly available at the NCBI Sequence Read Archive (SRA, http://www.ncbi.nlm.nih.gov/Traces/sra) under Project Accession number PRJNA589708.

RNA-Seq data from Cymbastela concentrica and Crella incrustans is available on request through Bioplatforms Australia (https://data.bioplatforms.com/organisation/about/australian-microbiome). Sample IDs are found in Supplementary File 1, Table S2.

MAGs can be accessed publicly via JGI GOLD (https://gold.jgi.doe.gov/), GOLD Analysis Project IDs can be found in Supplementary File 1, Table S6.

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Acknowledgements

The authors thank Mike Taylor for the T. stolonifera sequencing data, Michael Carnell for helpful advice and support for this study and Başak Öztürk and Bart Nijsse for previous work on Crambe crambe and data generation. We acknowledge Illumina and the Earth Microbiome Project for Crella incrustans metagenomic sequencing, including these individuals: Luke Thompson, Jon Sanders, Rodolfo Salido Benitez, Karenina Sanders, Caitriona Brennan, Jeremiah Minich, MacKenzie Bryant, Lindsay DeRight Goldasich, Greg Humphrey, and Rob Knight. For the generation of Cymbastela concentrica and Crella incrustans RNA-Seq data, we acknowledge the contribution of the Marine Microbes project, which was supported by funding from Bioplatforms Australia and the Integrated Marine Observing System (IMOS) through the Australian Government National Collaborative Research Infrastructure Strategy (NCRIS) in partnership with the Australian research community.

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This work was further supported by funds provided through the Australian Research Council and the Betty and Gordon Moore Foundation.

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Correspondence to Torsten Thomas.

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Taylor, J.A., Palladino, G., Wemheuer, B. et al. Phylogeny resolved, metabolism revealed: functional radiation within a widespread and divergent clade of sponge symbionts. ISME J (2020). https://doi.org/10.1038/s41396-020-00791-z

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