A genomic view of the microbiome of coral reef demosponges

Abstract

Sponges underpin the productivity of coral reefs, yet few of their microbial symbionts have been functionally characterised. Here we present an analysis of ~1200 metagenome-assembled genomes (MAGs) spanning seven sponge species and 25 microbial phyla. Compared to MAGs derived from reef seawater, sponge-associated MAGs were enriched in glycosyl hydrolases targeting components of sponge tissue, coral mucus and macroalgae, revealing a critical role for sponge symbionts in cycling reef organic matter. Further, visualisation of the distribution of these genes amongst symbiont taxa uncovered functional guilds for reef organic matter degradation. Genes for the utilisation of sialic acids and glycosaminoglycans present in sponge tissue were found in specific microbial lineages that also encoded genes for attachment to sponge-derived fibronectins and cadherins, suggesting these lineages can utilise specific structural elements of sponge tissue. Further, genes encoding CRISPR and restriction-modification systems used in defence against mobile genetic elements were enriched in sponge symbionts, along with eukaryote-like gene motifs thought to be involved in maintaining host association. Finally, we provide evidence that many of these sponge-enriched genes are laterally transferred between microbial taxa, suggesting they confer a selective advantage within the sponge niche and therefore play a critical role in host ecology and evolution.

Fig. 1. Phylogenetic tree showing all publicly available bacterial and archaeal MAGs and genomes (N = 1253 genomes) with >50% completeness and <10% contamination, recovered from 30 sponge species (Table S1).

Inner clade colour denotes phylum affiliation except for the Proteobacteria, which is split by class into alpha and gamma-proteobacteria. Outer tree colour strip identifies the sponge species from with the genome or MAG originated. Red stars indicate MAGs produced in this study.

Fig. 2. Phylogenetic tree showing the distribution of glycosyl hydrolases and esterases across MAGs with >85% completeness (N = 884).

Values represent the copy number of each gene per MAG. Internal branches of the tree are coloured by phylum, while the outer strip is coloured by class. Both are listed clockwise in the order in which they appear. Seawater MAGs are denoted by grey labels with red text.

Fig. 3. Phylogenetic tree showing the distribution of eukaryote-like repeat proteins—ankyrin (ARP), leucine-rich (LRR), tetratricopeptide (TPR), HEAT and WD40—across MAGS with >85% completeness (N = 884).

Values represent the percentage of coding genes per MAG devoted to each gene class. Internal branches of the tree are coloured by phylum, while the outer strip is coloured by class, and both are listed clockwise in the order in which they appear. MAGs from seawater are denoted by grey labels with red text.

Fig. 4. Phylogenetic tree showing the distribution of cadherins, fibronectins and fibronectin-binding proteins across MAGS with >85% completeness (N = 884).

Values represent the copy number of each gene per MAG. Internal branches of the tree are coloured by phylum while the outer strip is coloured by class. Both are listed clockwise in the order in which they appear. Seawater MAGs are denoted by grey labels with red text.

Fig. 5. Visualisation of LGTs detected within the MAGs for the five sponges passing the cumulative MAG length criteria (>100 Mbp).

The inner strip is coloured by phylum while the outer strip is coloured by host sponges. Bands connect donors and recipients, with their colour corresponding to the donors and the width correlating to the number of LGTs.

Fig. 6. Visualisation of gene flow among microbial phyla for gene families enriched in sponge-associated MAGs.

The inner ring and band connecting donor and recipient is coloured by protein family of the gene being transferred, with the width of the band correlating to the number of LGTs. Recipient MAGs are shown in grey. The outer ring is coloured by microbial phylum. Representation of RM and CAS gene LGTs can be found in Fig. S10.

Fig. 7. Schematic overview of microbial interactions with the host as inferred from the functional potential encoded by the sponge-associated microbial MAGs.

Fbn fibronectin, cdh cadherins, RM restriction-modification systems, CAS CRISPR-associated proteins, ELP eukaryotic-like repeat proteins, CE7 carbohydrate esterase family 7, GH33 glycosyl hydrolase family 33.