Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges

Abstract

Many marine sponges are hosts to dense and phylogenetically diverse microbial communities that are located in the extracellular matrix of the animal. The candidate phylum Poribacteria is a predominant member of the sponge microbiome and its representatives are nearly exclusively found in sponges. Here we used single-cell genomics to obtain comprehensive insights into the metabolic potential of individual poribacterial cells representing three distinct phylogenetic groups within Poribacteria. Genome sizes were up to 5.4 Mbp and genome coverage was as high as 98.5%. Common features of the poribacterial genomes indicated that heterotrophy is likely to be of importance for this bacterial candidate phylum. Carbohydrate-active enzyme database screening and further detailed analysis of carbohydrate metabolism suggested the ability to degrade diverse carbohydrate sources likely originating from seawater and from the host itself. The presence of uronic acid degradation pathways as well as several specific sulfatases provides strong support that Poribacteria degrade glycosaminoglycan chains of proteoglycans, which are important components of the sponge host matrix. Dominant glycoside hydrolase families further suggest degradation of other glycoproteins in the host matrix. We therefore propose that Poribacteria are well adapted to an existence in the sponge extracellular matrix. Poribacteria may be viewed as efficient scavengers and recyclers of a particular suite of carbon compounds that are unique to sponges as microbial ecosystems.

Figure 1

Phylogenetic maximum-likelihood tree based on 16S rRNA genes of the candidate phylum Poribacteria. Sequences from poribacterial SAGs are shown in bold and gray shading. The tree was constructed based on long sequences (⩾1100 nucleotides), shorter sequences were added without changing tree topology and are indicated by dashed lines. Bootstrap support (1000 resamplings) of ⩾90% is shown by filled, and ⩾75% by open circles. The outgroup consisted of several Spirochaetes sequences. Scale bar represents 4% sequence divergence.

Figure 2

Schematic reconstruction of inositol degradation as encoded on poribacterial SAGs. Numbers within circles represent the number of genomes encoding for the corresponding enzyme.

Figure 3

Schematic reconstruction of uronic acid degradation as encoded on poribacterial SAGs. Numbers within circles represent the genomes encoding for the corresponding enzyme. Dashed circles represent manually annotated genes.

Figure 4

Schematic overview of a poribacterial cell in the sponge extracellular matrix illustrating pathways of carbohydrate metabolism and glycosaminoglycan degradation by poribacterial enzymes. The dashed arrow represents glycolysis that is not supported by the dominant poribacterial phylotype group I.