Characterization of a sponge microbiome using an integrative genome-centric approach

Abstract

Marine sponges often host diverse and species-specific communities of microorganisms that are critical for host health. Previous functional genomic investigations of the sponge microbiome have focused primarily on specific symbiont lineages, which frequently make up only a small fraction of the overall community. Here, we undertook genome-centric analysis of the symbiont community in the model species Ircinia ramosa and analyzed 259 unique, high-quality metagenome-assembled genomes (MAGs) that comprised 74% of the I. ramosa microbiome. Addition of these MAGs to genome trees containing all publicly available microbial sponge symbionts increased phylogenetic diversity by 32% within the archaea and 41% within the bacteria. Metabolic reconstruction of the MAGs showed extensive redundancy across taxa for pathways involved in carbon fixation, B-vitamin synthesis, taurine metabolism, sulfite oxidation, and most steps of nitrogen metabolism. Through the acquisition of all major taxa present within the I. ramosa microbiome, we were able to analyze the functional potential of a sponge-associated microbial community in unprecedented detail. Critical functions, such as carbon fixation, which had previously only been assigned to a restricted set of sponge-associated organisms, were actually spread across diverse symbiont taxa, whereas other essential pathways, such as ammonia oxidation, were confined to specific keystone taxa.

Fig. 1. Combined archaeal and bacterial phylogenetic tree based on single copy marker proteins (inferred with GTDB).

Labels colored in red are MAGs retrieved from this study. Black labels are previously published sponge symbiont genomes (MAGs, SAGs, and isolate genomes). Branch labels display taxonomy at the lowest inferred level. Genomes “GB_GCA_000522425.1” and “RS_GCF_900079095.1” were taxonomically uncharacterized by GTDB-Tk v0.2.2 (https://github.com/Ecogenomics/GtdbTk) and published taxonomy was used (Ca. Entotheonella factor [97] and Ca. Entotheonella palauensis [43], respectively). The bacterial and archaeal tree are rooted to LS-NOB (GB_GCA_001542995.1) and Nitrosopumilus (GCA_001543015.1), respectively.

Fig. 2. Metabolic reconstruction and proposed exchange of carbon, nitrogen, sulfur, and vitamins between Ircinia ramosa symbionts and the host.

HP-HB cycle: 3-hydroxypropionate/4-hydroxybutyrate cycle. Lineages in bold within the taurine metabolism box contain both genes encoding for the taurine transporter (tauACB) and taurine dioxygenase (tauD). Numbers in brackets within the vitamin metabolism stand for the metabolic potential to synthesize one or more of the following B-vitamins: 1: Biotin, 2: Cobalamin, 3: Pantothenate, 4: Pyridoxine, 5: Riboflavin, 6: Thiamine. See Fig. S13 for I. ramosa morphology.