Journal article Open Access

Marine Sponges as Chloroflexi Hot Spots: Genomic Insights and High-Resolution Visualization of an Abundant and Diverse Symbiotic Clade

Bayer, Kristina; Jahn, Martin T; Slaby, Beate M; Moitinho-Silva, Lucas; Hentschel, Ute


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    <subfield code="a">ACKNOWLEDGEMENTS. We acknowledge Laura Rix and Lucia Pita Galan for many insightful discussions on sponge ecology and Sebastian M. Markert and Christian Stigloher at University of Wuerzburg for help with FISH-CLEM.

This study was supported by DFG (CRC1182-TPB1) and European Union's Horizon 2020 research and innovation program grants (679849 SponGES). M.T.J. was supported by a grant of the German Excellence Initiative to the Graduate School of Life Sciences, University of Wuerzburg. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.</subfield>
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    <subfield code="a">&lt;p&gt;&lt;strong&gt;ABSTRACT &lt;/strong&gt;Members of the widespread bacterial phylum &lt;em&gt;Chloroflexi &lt;/em&gt;can dominate high-microbial-abundance (HMA) sponge microbiomes. In the Sponge Microbiome Project, &lt;em&gt;Chloroflexi &lt;/em&gt;sequences amounted to 20 to 30% of the total microbiome of certain HMA sponge genera with the classes/clades SAR202, &lt;em&gt;Caldilineae&lt;/em&gt;, and &lt;em&gt;An- aerolineae &lt;/em&gt;being the most prominent. We performed metagenomic and single- cell genomic analyses to elucidate the functional gene repertoire of &lt;em&gt;Chloroflexi &lt;/em&gt;symbionts of &lt;em&gt;Aplysina aerophoba&lt;/em&gt;. Eighteen draft genomes were reconstructed and placed into phylogenetic context of which six were investigated in detail. Common genomic features of &lt;em&gt;Chloroflexi &lt;/em&gt;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 &lt;em&gt;Anaerolineae &lt;/em&gt;and &lt;em&gt;Caldilineae &lt;/em&gt;ge- nomes, but only amino acid utilization by SAR202. While &lt;em&gt;Anaerolineae &lt;/em&gt;and &lt;em&gt;Caldilin- eae &lt;/em&gt;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. &lt;em&gt;Chloroflexi &lt;/em&gt;symbionts were visualized in the sponge extracellular matrix at ultrastructural resolution by the fluorescence &lt;em&gt;in situ &lt;/em&gt;hybridization-correlative light and electron microscopy (FISH-CLEM) method. Carbo- hydrate degradation potential was reported previously for &amp;ldquo;&lt;em&gt;Candidatus &lt;/em&gt;Poribacteria&amp;rdquo; 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.&lt;/p&gt;

&lt;p&gt;&lt;strong&gt;I M P O R T A N C E &lt;/strong&gt;&lt;em&gt;Chloroflexi &lt;/em&gt;represent a widespread, yet enigmatic bacterial phylum with few cultivated members. We used metagenomic and single-cell genomic ap- proaches to characterize the functional gene repertoire of &lt;em&gt;Chloroflexi &lt;/em&gt;symbionts in marine sponges. The results of this study suggest clade-specific metabolic specializa- tion and that &lt;em&gt;Chloroflexi &lt;/em&gt;symbionts have the genomic potential for dissolved organic matter (DOM) degradation from seawater. Considering the abundance and domi- nance of sponges in many benthic environments, we predict that the role of sponge symbionts in biogeochemical cycles is larger than previously thought.&lt;/p&gt;</subfield>
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