Physiological plasticity in a Moorean phototrophic sponge is decoupled from microbiome shifts

Abstract

Sponges are prominent members of coral reef communities and contribute to nutrient cycling through multiple pathways. Many reef sponges host abundant microbial symbionts, including photosymbionts that can drive substantial carbon and nitrogen uptake and processing within the holobiont, likely reducing host dependence on other resource pools. While species-specific microbiome composition and holobiont physiology are increasingly well characterized, fine-scale intraspecific variation within reef populations remains comparatively understudied. Here we investigated physiological and microbiome differences in the phyllosponge Lendenfeldia chondrodes across three shallow reef habitats along the northern shore of Moorea, French Polynesia. Using stable isotope tracers, net primary productivity (NPP) measurements, chlorophyll a analysis, and 16S rRNA amplicon sequencing, we quantified carbon fixation, isotopic enrichment, photosymbiont abundance, and microbiome composition for sponges collected across three sites ranging from 2 to 10 m depth. NPP varied significantly among sites and, when modeled against published NPP/P:R relationships, confirm a strong phototrophic capacity in L. chondrodes. This, along with variation across sites in NPP, isotope values, and Chlorophyll a concentration in sponge tissue, indicate that carbon and nitrogen uptake and fixation differ meaningfully across these small spatial scales. Microbiome composition also differed among sites, with sponges collected in Opunohu Bay—where a distinct encrusting morphotype was observed—harboring more diverse and compositionally distinct microbial communities. Critically, patterns of microbiome divergence and physiological divergence were decoupled: metabolic differences were most pronounced at the Intercontinental Resort site, while microbial differences were greatest at Opunohu Bay. This decoupling suggests that shifts in holobiont function can occur without corresponding restructuring of microbial symbiont communities, potentially reflecting functional redundancy within the microbiome, strong host regulation of physiological processes, or rapid metabolic responses to local environmental conditions. Together, these findings indicate that L. chondrodes exhibits meaningful intraspecific physiological plasticity across fine spatial scales. This metabolic flexibility may generate spatial heterogeneity in benthic primary productivity and nutrient cycling across reef habitats, with broader implications for carbon retention and ecosystem resilience.