Abstract

Background. Color polymorphism is common in marine sponges, but the mechanisms driving color variation remain unclear. This study investigated environmental and microbial drivers of color polymorphism in the marine sponge Halichondria panicea, which exhibits green and yellow morphs.

Methods. A total of 105 sponge samples (42 green and 63 yellow) were collected from three locations with varying bathing water quality and over four seasons. Analyses included microbiome profiling (16S and 18S ribosomal RNA (rRNA) variable V3/V4 region amplicon sequencing), pigment quantification, PICRUSt2-based functional prediction, and comprehensive seawater physical and chemical measurements. The study evaluated drivers of color variation, mainly testing the surrounding environmental factors that may contribute to shaping the sponge's photosymbiotic bacterial community.

Results. Green morphs represented stable, photosymbiont-rich communities dominated by Acaryochloris MBIC11017, with significantly higher chlorophyll and carotenoid concentrations, elevated cyanobacterial diversity, phototrophic eukaryotes (Phymatolithon), and enhanced metabolic profiles characterized by anaerobic metabolism, specialized metal transport systems, and sulfur cycling pathways. Yellow morphs represented stress-adapted, heterotroph-dominated states with Synechococcus CC9902 dominance, reduced pigment content, lower cyanobacterial diversity, increased parasitic dinoflagellate abundance (Syndiniales), and simplified metabolic profiles enriched in oxidative, stress-responsive pathways. Multiple statistical approaches (Random Forest, elastic net) all identified conductivity, nutrients (ammonium, nitrite), pH, and heavy metals as primary drivers. Green morphs were found in moderate metal environments with alkaline pH and lower ionic stress. Yellow morphs dominated high conductivity, elevated total dissolved solids, and nutrient-enriched conditions. Sponge color distribution was independent of bathing water quality classifications and season, but varied significantly by location.

Conclusions. Color polymorphism reflects distinct holobiont states shaped by the surrounding environmental conditions. Green morphs represent stable communities with complex photosymbiotic bacteria, while yellow morphs represent stress-adapted communities with simplified metabolic profiles. Both morphs are functional, but the yellow morphs may be less resilient to additional stressors. Therefore, sponge color serves as a bioindicator of environmental stress conditions and holobiont state, providing insights into sponge responses to environmental change.