A partner-resolved marine sponge hologenome reveals that three bacterial symbionts disproportionately expand holobiont metabolism via enriched membrane transporter repertoires

Marine sponges associate with microbial symbionts that shape host physiology and drive nutrient cycling, yet assigning partner-specific contributions to holobiont metabolism remains challenging in species with complex microbiomes. The coral reef demosponge Amphimedon queenslandica offers tractable resolution, as its adult microbiome is dominated by just three extracellular, vertically inherited gammaproteobacterial symbionts (AqS1, AqS2 and AqS3). Here, we present improve genome assemblies of the host and each symbiont, integrated with adult holotranscriptomes to resolve functional partitioning and expressed pathway capacity of each partner. Despite representing only [~]20% of KEGG-annotated hologenome genes, the three symbionts contribute 45.2 and 72% of metabolic and membrane transporter genes, respectively, revealing a pronounced functional imbalance in proteins involved in nutrient transformation and exchange. Although central heterotrophic carbon metabolism is complete across all four partners, gene content and expression are consistent with symbiont uptake of host-liberated carbohydrates. Complementation of pathways occurs across dissolved inorganic nutrient assimilation, including nitrate reduction, sulfur redox metabolism, and phosphate uptake and storage. Symbionts further expand holobiont biosynthetic breadth through amino acid, vitamin, and co-factor pathways that are incomplete or absent from the host, coupled with expressed membrane transporter repertoires consistent with directed metabolite exchange. Together, these results show that vertically inherited symbionts can disproportionately expand holobiont metabolic capacity, with membrane transporter enrichment linking symbiont metabolic breadth to host physiology. This exchange-oriented functional architecture, rather than simple pathway redundancy, appears to underlie metabolic integration in this low-complexity animal- microbe symbiosis.