Hypothesis

Ocean acidification (OA) modifies the carbohydrate composition of coral surface mucus, reducing the abundance of sulfated glycans that normally bind beneficial viruses and bacteria. This loss of glycan‑mediated recruitment diminishes viral lysis of opportunistic microbes and impairs colonization of mutualistic bacteria such as Endozoicomonas. Consequently, nutrient flux (especially B‑vitamins and fixed nitrogen) from the microbiome to the intracellular Symbiodiniaceae declines, forcing the symbiont to rely more heavily on host‑derived carbon and pushing the partnership along the mutualism‑parasitism continuum toward a parasitic state.

Mechanistic Basis

Coral mucus is a glycoprotein‑rich matrix whose glycan profile determines which microorganisms can adhere and persist. Prior work shows that sulfated fucans and mannose‑rich glycans serve as receptors for marine bacteriophages and for beneficial bacteria that provide vitamins B1 and B6 and nitrogen to symbionts [1][2]. OA lowers seawater pH and carbonate ion concentration, which can affect the activity of glycosyltransferases and sulfotransferases in the mucus‑producing epidermis, leading to under‑sulfation and altered monosaccharide composition. When these glycans are depleted, phage adsorption rates drop, reducing top‑down control of bacterial populations, and bacterial attachment sites are lost, weakening the mutualistic microbiome.

Symbiodiniaceae rely on bacterial‑derived vitamins and nitrogen for efficient photosynthesis and carbon translocation to the host [1]. A reduction in these supplies lowers the symbiont’s photosynthetic output, decreasing the carbon available for host calcification and increasing the host’s reliance on heterotrophic feeding. Under energetic stress, the symbiont may begin to consume host‑derived lipids or amino acids, shifting the interaction from mutualistic to parasitic.

Testable Predictions

1. Corals exposed to OA‑level pH (7.8) will exhibit a measurable decrease in sulfated glycans and mannose residues in their mucus compared to ambient pH (8.1) controls.
2. Viral adsorption to mucus will be significantly lower under OA conditions, quantified by fluorescently labeled phage binding assays.
3. Abundance of Endozoicomonas and other vitamin‑providing bacteria in the mucus layer will decline under OA, as shown by 16S rRNA amplicon sequencing.
4. Intracellular Symbiodiniaceae will show reduced B‑vitamin and nitrogen transporter expression and lower ^13C‑bicarbonate fixation rates when hosted by OA‑treated corals.
5. The net carbon translocation from symbiont to host will decrease, and symbiont cells will display increased lipid accumulation or autophagy markers indicative of a shift toward parasitic metabolism.

Experimental Approach

• Mucus Glycome Analysis: Collect mucus from nubbins of Acropora millepora maintained at ambient (pH 8.1) and OA (pH 7.8) conditions for 4 weeks. Perform LC‑MS/MS of released glycans after mild acid hydrolysis to quantify sulfated fucans, mannose, and galactose residues.
• Virus Binding Assay: Incubate mucus aliquots with SYBR‑green labeled marine phage isolates; measure bound fluorescence via flow cytometry to calculate adsorption efficiency.
• Microbiome Profiling: Extract DNA from mucus and tissue; sequence V4 region of 16S rRNA. Quantify relative abundance of Endozoicomonas and other known beneficial taxa.
• Symbiont Physiology: Isolate Symbiodiniaceae from host tissue; conduct qPCR for vitamin B1/B6 transporters and nitrogen assimilation genes (e.g., amt, glnA). Perform ^13C‑bicarbonate pulse‑chase experiments to assess photosynthetic fixation and translocation to host tissue measured by IRMS.
• Metabolic Shift Indicators: Use transmission electron microscopy to detect lipid droplet accumulation and autophagosome formation in symbiont cells; quantify via image analysis.

Statistical comparisons (ANOVA with post‑hoc Tukey) will test whether OA significantly alters each measured variable. Confirmation of the predicted directional changes would support the hypothesis; lack of significant differences in mucus glycome, virus binding, beneficial bacteria, or symbiont metabolic markers would falsify it.

This framework links carbonate chemistry to molecular glycan alterations, microbiome‑virus dynamics, and symbiont physiology, providing a concrete, falsifiable pathway by which OA may destabilize the coral holobiont before overt bleaching or calcification loss occurs.