Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges

Abstract

In this study, we present a single-cell genomics approach for the functional characterization of the candidate phylum Poribacteria, members of which are nearly exclusively found in marine sponges. The microbial consortia of the Mediterranean sponge Aplysina aerophoba were singularized by fluorescence-activated cell sorting, and individual microbial cells were subjected to phi29 polymerase-mediated 'whole-genome amplification'. Pyrosequencing of a single amplified genome (SAG) derived from a member of the Poribacteria resulted in nearly 1.6 Mb of genomic information distributed among 554 contigs analyzed in this study. Approximately two-third of the poribacterial genome was sequenced. Our findings shed light on the functional properties and lifestyle of a possibly ancient bacterial symbiont of marine sponges. The Poribacteria are mixotrophic bacteria with autotrophic CO 2 -fixation capacities through the Wood-Ljungdahl pathway. The cell wall is of Gram-negative origin. The Poribacteria produce at least two polyketide synthases (PKSs), one of which is the sponge-specific Sup-type PKS. Several putative symbiosis factors such as adhesins (bacterial Ig-like domains, lamininin G domain proteins), adhesin-related proteins (ankyrin, fibronectin type III) and tetratrico peptide repeat domain-encoding proteins were identified, which might be involved in mediating sponge-microbe interactions. The discovery of genes coding for 24-isopropyl steroids implies that certain fossil biomarkers used to date the origins of metazoan life on earth may possibly be of poribacterial origin. Single-cell genomic approaches, such as those shown herein, contribute to a better understanding of beneficial microbial consortia, of which most members are, because of the lack of cultivation, inaccessible by conventional techniques.

Deep sequencing of non-ribosomal peptide synthetases and polyketide synthases from the microbiomes of Australian marine sponges

“…(Fan et al, 2012) using the mWGS technique. However, the TEFAP approach detected sup type KS domains, which are thought to be limited to poribacterial species (Hochmuth and Piel, 2009;Siegl and Hentschel, 2010;Siegl et al, 2011). The detection of sup domains at very low abundance has also been reported within the marine sponge Arenosclera brasiliensis (Trindade-Silva et al, 2012).…”

“…This co-occurrence of these two domain types was also observed from the sponge Cacospongia mycofijiensis (Fieseler et al, 2007;Hochmuth et al, 2010), which belongs to the same order as R. odorabile. The occurrence of these sup type KS domains in R. odorabile coincided with the detection of poribacteria (Fan et al, 2012), which are known to harbour the sup biosynthetic gene cluster (Siegl and Hentschel, 2010;Siegl et al, 2011). The calculated richness index (Table 2), indicated a moderate number of sup KS domains within the microbiome of this sponge.…”

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

“…The Candidatus Poribacteria symbiont in sponges has the genomic potential for both ferric iron and heme uptake (Siegl et al, 2010), Candidatus Endoriftia persephone, the symbiont in tubeworms, can uptake both ferrous and ferric iron (Robidart et al, 2008), whereas Teredinibacter turnerae, the symbiont of wood-feeding bivalves, appears to possess only a single hemin-based mechanism for iron uptake (Yang et al, 2009). Until additional data is available for other beneficial symbionts, it remains unknown whether multiple modes of iron acquisition are an adaptation broadly employed by symbionts.…”

Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges

“…Additionally, certain sponge symbionts produce secondary metabolites that might be involved in the chemical defense of their hosts (Kennedy et al, 2007;Siegl and Hentschel 2010;Thomas et al, 2010a). Genomic information is currently being used to further characterize features of symbiosis and physiological properties and the lifestyle of sponge symbionts (Hochmuth et al, 2010;Thomas et al, 2010b;Siegl et al, 2011).…”