Host-mediated oxidative primingselects for rare microbiome taxa that buffer calcification under combined thermal and acidification stress

Hypothesis

Host cells under combined thermal and acidification stress increase production of reactive oxygen species (ROS) that selectively enrich rare microbiome taxa capable of degrading host-derived antioxidant compounds, thereby modulating the redox environment at the calcifying interface and preserving calcification rates.

Mechanistic basis

• Thermal stress triggers Symbiodiniaceae expulsion and ROS generation (see Oxidative Theory of Coral Bleaching) [https://pmc.ncbi.nlm.nih.gov/articles/PMC12835581/].
• Ocean acidification lowers pH, reducing carbonate ion availability and upregulating host proton pumps, which further elevates intracellular ROS via mitochondrial stress.
• Host ROS act as signaling molecules that upregulate expression of mucin-like glycoproteins and antimicrobial peptides, creating a niche favoring rare bacteria equipped with catalase, peroxidase, or alternative oxidase genes (e.g., rare Rhodobactereae and Microtrichales lineages).
• These rare taxa metabolize host-derived ROS and exude bicarbonate or organic carbon that can be transferred to the calcifying epithelium, locally raising pH and Ωaragonite.
• Consequently, corals with a microbiome enriched in ROS-scavenging rare taxa maintain higher calcification under combined stress, while those lacking this consortium show accelerated skeletal degradation.

Testable predictions

1. Exposing Acropora fragments to elevated temperature (+2°C) and low pH (pH 7.8) will increase host ROS levels measured by DCFDA fluorescence within 48 h.
2. 16S rRNA amplicon sequencing will reveal a significant rise in relative abundance of rare (<0.1% of community) bacterial OTUs possessing antioxidant genes (identified via metagenomic screening) compared to ambient controls.
3. Inhibiting host ROS production with the antioxidant N-acetylcysteine will blunt the enrichment of these rare taxa and reduce calcification rates relative to untreated stressed fragments.
4. Re-inoculating stressed fragments with a cultured consortium of ROS-degrading rare isolates will rescue calcification to near-control levels, whereas inoculating with a control bacterial mix will not.

Potential pitfalls

• Rare taxa may be below detection limits; using spike-in standards and long-read metagenomics can improve sensitivity.
• ROS measurements must be compartment-specific (surface mucus vs. tissue) to avoid confounding signals from symbiont photosynthesis.
• Scaling from fragment experiments to whole colonies requires accounting for flow-dependent nutrient exchange.

If falsified—i.e., no correlation between host ROS, rare taxon enrichment, and calcification preservation—then the hypothesis that host-driven oxidative priming selects for protective rare microbes would be rejected, prompting focus on alternative mechanisms such as direct ion-transport regulation or symbiont-mediated carbon recycling.