Abstract
The endemic marine sponge Arenosclera brasiliensis (Porifera, Demospongiae, Haplosclerida) is a known source of secondary metabolites such as arenosclerins A-C. In the present study, we established the composition of the A. brasiliensis microbiome and the metabolic pathways associated with this community. We used 454 shotgun pyrosequencing to generate approximately 640,000 high-quality sponge-derived sequences (∼150 Mb). Clustering analysis including sponge, seawater and twenty-three other metagenomes derived from marine animal microbiomes shows that A. brasiliensis contains a specific microbiome. Fourteen bacterial phyla (including Proteobacteria, Cyanobacteria, Actinobacteria, Bacteroidetes, Firmicutes and Cloroflexi) were consistently found in the A. brasiliensis metagenomes. The A. brasiliensis microbiome is enriched for Betaproteobacteria (e.g., Burkholderia) and Gammaproteobacteria (e.g., Pseudomonas and Alteromonas) compared with the surrounding planktonic microbial communities. Functional analysis based on Rapid Annotation using Subsystem Technology (RAST) indicated that the A. brasiliensis microbiome is enriched for sequences associated with membrane transport and one-carbon metabolism. In addition, there was an overrepresentation of sequences associated with aerobic and anaerobic metabolism as well as the synthesis and degradation of secondary metabolites. This study represents the first analysis of sponge-associated microbial communities via shotgun pyrosequencing, a strategy commonly applied in similar analyses in other marine invertebrate hosts, such as corals and algae. We demonstrate that A. brasiliensis has a unique microbiome that is distinct from that of the surrounding planktonic microbes and from other marine organisms, indicating a species-specific microbiome.
Highlights
Sponges are probably the most primitive metazoans, with fossil records for this group dating from 635 to 750 million years ago [1]
Another possibility is that A. brasiliensis-associated facultatively anaerobic Proteobacteria harbor oxygen-tolerant carbon monoxide dehydrogenase (CODH) and formate dehydrogenase (FDH) enzymes to carry out thermodynamically favored oxidative processes involved in energy and CO2 generation
We show that the A. brasiliensis microbiome is unique, differing from the microbiomes present in the water column surrounding these sponges and those associated with other marine organisms
Summary
Sponges are probably the most primitive metazoans, with fossil records for this group dating from 635 to 750 million years ago [1]. Based on 16S rRNA identification (97% identity cutoff), only thirty-four different OTUs were common between C. concentrica and the surrounding seawater, supporting the idea of selection for a specific microbiome, possibly consisting of several (though non-culturable) bacteria. The sponge metagenomes contained a greater number of sequences identified as COG0610 (restriction enzymes, type I helicase) and COG1715 (restriction endonuclease) than the surrounding seawater. Both COG groups include specific DNA modification and restriction systems in bacteria, and the authors hypothesized that this would facilitate horizontal DNA exchange between sponge microorganisms and protect against DNA exchange with planktonic organisms in the surrounding seawater [10]
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