Taxonomic and Functional Microbial Signatures of the Endemic Marine Sponge Arenosclera brasiliensis

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.

Polyketide Synthase Gene Diversity within the Microbiome of the Sponge Arenosclera brasiliensis, Endemic to the Southern Atlantic Ocean

“…The production of manzamine A, an alkaloid found in several haplosclerid sponges, has been assigned to an Actinomycetales strain of the genus Micromonospora (12). Furthermore, our previous metagenomic analysis indicated that Actinobacteria was one of the most abundant bacterial phyla in the microbiome associated with A. brasiliensis (29). Therefore, it is reasonable to suggest that A. brasiliensis-associated Actinobacteria communities might be responsible for the production of secondary metabolites as well as of bioactive polyketides.…”

“…Specimens of A. brasiliensis were collected at João Fernandinho's Beach, which is located in the Búzios peninsula in the state of Rio de Janeiro (22°44=49==/41°52=54==W), during two expeditions in May 2010 and January 2011. Sponge specimens were transported under controlled temperature (24°C) in aerated seawater for approximately 3 h and then washed and processed for total DNA extraction exactly as previously described (29). Briefly, samples were set on sterile seawater for 5 to 10 min, dissected with a sterile scalpel, dried by gently pressing on sterile paper towels, and ground in liquid nitrogen.…”

“…The raw input and the assembled sequences of KS amplicon pyrosequencing data are available at the MG-RAST server under project "Arenosclera brasiliensis_PKS diversity." The sequence data of A. brasiliensis metagenomes is also available under project "Arenosclera brasiliensis_Metagenome" (29). The sequences of KS contigs were deposited into GenBank under accession numbers JX012425 to JX012657 (contigs from amplicon pyrosequencing) and JX945643 (contig from sponge metagenome shotgun pyrosequencing).…”

GenomePeek - An online tool for prokaryotic and metagenome analysis

“…While complete genome sequencing gives us detailed knowledge about a single prokaryotic species, metagenomic sequencing gives as a broad overview of the microbial environment (Dinsdale et al, 2008). Whether analyzing genomic or metagenomic sequencing, one of the main goals is to identify the taxonomic origin of species or species (Belda-Ferre et al, 2012;Mande, Mohammed, & Ghosh, 2012;Trindade-Silva et al, 2012;Carr, Shen-Orr, & Borenstein, 2013).…”

“…While complete genome sequencing gives us detailed knowledge about a single prokaryotic species, metagenomic sequencing gives as a broad overview of the microbial environment (Dinsdale et al, 2008). Whether analyzing genomic or metagenomic sequencing, one of the main goals is to identify the taxonomic origin of species or species (Belda-Ferre et al, 2012;Mande, Mohammed, & Ghosh, 2012;Trindade-Silva et al, 2012;Carr, Shen-Orr, & Borenstein, 2013).There are two typical approaches to identifying the species present in a metagenome. The most common methods use homology searches against a reference database of known taxonomic lineage (Altschul et al, 1997;Meyer et al, 2008;Segata et al, 2012).…”