Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis

Abstract

Sponges form close relationships with bacteria, and a remarkable phylogenetic diversity of yet-uncultured bacteria has been identified from sponges using molecular methods. In this study, we use a comparative metagenomic analysis of the bacterial community in the model sponge Cymbastela concentrica and in the surrounding seawater to identify previously unrecognized genomic signatures and functions for sponge bacteria. We observed a surprisingly large number of transposable insertion elements, a feature also observed in other symbiotic bacteria, as well as a set of predicted mechanisms that may defend the sponge community against the introduction of foreign DNA and hence contribute to its genetic resilience. Moreover, several shared metabolic interactions between bacteria and host include vitamin production, nutrient transport and utilization, and redox sensing and response. Finally, an abundance of protein-protein interactions mediated through ankyrin and tetratricopeptide repeat proteins could represent a mechanism for the sponge to discriminate between food and resident bacteria. These data provide new insight into the evolution of symbiotic diversity, microbial metabolism and host-microbe interactions in sponges.

Functional genomic analysis of an uncultured δ-proteobacterium in the sponge Cymbastela concentrica

“…A novel d-proteobacterial clade of sponge-associated bacteria In the phylogenetic survey of the bacterial community associated with the sponge C. concentrica, we discovered a 16S rRNA gene sequence (Thomas et al, 2010) that was assigned by the Ribosomal Database Project classifier to the class d-proteobacteria (87% confidence) and the order of Bdellovibrionales (81% confidence). Phylogenetic analysis and comparison of the sponge d-proteobacterial sequence with sequences from closely related isolates and uncultured organisms ( Figure 1) showed that it falls into a cluster of uncultured bacteria that were all found in marine sponges.…”

“…Functional genomic comparison of the sponge d-proteobacterium with related bacteria To gain insight into the functional genomic properties of the new d-proteobacterium, we reconstructed a partial genome for the organism from data of our recent metagenomic study (Thomas et al, 2010). The assembled data represent a composite genome of many related individuals as seen in other partial genome reconstructions from metagenomic shotgun data (for example, Tyson et al, 2004;Hallam et al, 2006) and within population variation may exist at the single-nucleotide or gene level.…”

“…Binning of scaffolds with 420 kb sequence was done according to a modification of the strategy outlined by Woyke et al (2006) and Thomas et al (2010) and is further described in the Supplementary Information.…”

“…The partial genome of the d-proteobacterial species was re-constructed by binning of shotgun-sequencing data from the bacterial community of the sponge C. concentrica (Thomas et al, 2010). Binning of scaffolds with 420 kb sequence was done according to a modification of the strategy outlined by Woyke et al (2006) and Thomas et al (2010) and is further described in the Supplementary Information.…”

“…We have recently applied whole-environment shotgun sequencing to characterize the bacterial community of the sponge Cymbastela concentrica, an abundant sponge species in shallow, temperate waters along the Australian east coast (Thomas et al, 2010). This metagenomic study has revealed previously unrecognized genomic signatures and functions of sponge bacteria including defense mechanisms against the introduction of foreign DNA, metabolic interactions with the host through vitamin production, nutrient transport and utilization, redox sensing and response, as well as proteinprotein interactions mediated through ankyrin and tetratricopeptide repeat (TPR) proteins.…”