Journal article Open Access

Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization

Slaby, Beate; Hackl, Thomas; Horn, Hannes; Bayer, Kristina; Hentschel, Ute

Marine sponges are ancient metazoans that are populated by distinct and highly diverse microbial communities. In order to obtain deeper insights into the functional gene repertoire of the Mediterranean sponge Aplysina aerophoba, we combined Illumina short-read and PacBio long-read sequencing followed by un-targeted metagenomic binning. We identified a total of 37 high-quality bins representing 11 bacterial phyla and two candidate phyla. Statistical comparison of symbiont genomes with selected reference genomes revealed a significant enrichment of genes related to bacterial defense (restriction-modification systems, toxin-antitoxin systems) as well as genes involved in host colonization and extracellular matrix utilization in sponge symbionts. A within-symbionts genome comparison revealed a nutritional specialization of at least two symbiont guilds, where one appears to metabolize carnitine and the other sulfated polysaccharides, both of which are abundant molecules in the sponge extracellular matrix. A third guild of symbionts may be viewed as nutritional generalists that perform largely the same metabolic pathways but lack such extraordinary numbers of the relevant genes. This study characterizes the genomic repertoire of sponge symbionts at an unprecedented resolution and it provides greater insights into the molecular mechanisms underlying microbial-sponge symbiosis.

This project was funded by Grant Number CSP1291 of the DOE Joint Genome Institute, the European Commission within its FP7 Program, under the thematic area KBBE.2012.3.2.-01 with Grant Number 311932 ('SeaBio-Tech'), and by the European Union's Horizon 2020 research and innovation program under Grant Agreement No. 679849 ('SponGES'). BMS was supported by a grant of the German Excellence Initiative to the Graduate School of Life Sciences, University of Würzburg. We thank Monika Bright (University of Vienna) and the Marine Biology Station Piran for support during sampling, Tanja Woyke (DOE Walnut Creek, CA, USA) for helpful discussions on differential coverage binning, Martin Jahn (GEOMAR) for suggestions on the interrogations of the amplicon data, as well as Frank Förster and Thomas Dandekar (Department of Bioinformatics, University of Würzburg, Würzburg, Germany) for useful advice and access to their servers. © The Author(s) 2017. This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http:// creativecommons.org/licenses/by/4.0/
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