Hypothesis

We propose that the combined stress of ocean acidification (OA) and elevated temperature impairs Ca²⁺‑ATPase function in coral calicoblastic cells, reducing intracellular Ca²⁺ buffering capacity. This deficit triggers a compensatory increase in heterotrophic feeding on particulate organic matter (POM) to fuel Ca²⁺‑binding proteins (e.g., calmodulin) that mitigate acidification‑induced calcification decline. The heightened heterotrophic flux selects for specific bacterial taxa capable of hydrolyzing complex POM (e.g., chitin‑degrading Flavobacteria), which in turn supply the host with usable nutrients and reinforce the feedback loop. When the microbiome cannot reorganize to support sufficient heterotrophic processing, calcification collapses.

Mechanistic Basis

OA directly disrupts Ca²⁺ homeostasis by lowering aragonite saturation and inhibiting Ca²⁺‑ATPase activity【https://pmc.ncbi.nlm.nih.gov/articles/PMC12167964/】. Thermal stress exacerbates this by increasing metabolic demand and promoting microbiome functional reorganization, marked by rises in rare taxa and alpha/beta diversity【https://www.frontiersin.org/journals/marine-science/articles/10.3389/fmars.2025.1635356/full】. Corals already exhibit seasonal trophic plasticity, shifting toward heterotrophy under stress【https://academic.oup.com/ismecommun/article/5/1/ycae162/8078337】. We argue that this plasticity is not merely a passive response but an active, microbiome‑mediated strategy to sustain Ca²⁺‑dependent calcification when ion transporters are compromised. Core microbiome members may provide stability, while transient heterotroph‑associated bacteria supply enzymatic capacity to extract calcium‑rich compounds from POM, thereby indirectly supporting the calcifying machinery.

Testable Predictions

1. Under OA + heat conditions, corals with experimentally enhanced heterotrophic feeding rates will maintain higher calcification rates than unfed controls, whereas feeding enhancement will have little effect under OA or heat alone.
2. Blocking heterotrophic uptake (e.g., using size‑exclusion filters) will accelerate calcification decline specifically in the OA + heat treatment, not in single‑stressor treatments.
3. Metagenomic sequencing will reveal a consistent enrichment of bacterial families possessing extracellular enzyme genes (e.g., chitinases, proteases) in corals that preserve calcification under OA + heat.
4. Pharmacological inhibition of calmodulin or other Ca²⁺‑binding proteins will abolish the protective effect of heterotrophic feeding on calcification, even when feeding rates are high.

Experimental Approach

• Maintain nubbins of a model coral (e.g., Acropora spp.) in factorial aquaria: control, OA (pH 7.8), heat (+2 °C), and OA + heat.
• Within each condition, manipulate heterotrophic access: (a) open flow (natural particulate supply), (b) filtered flow (0.2 µm to remove POM), (c) supplemented POM (addition of isotopically labeled Artemia nauplii).
• Measure calcification buoyant weight, Ca²⁺‑ATPase expression (qPCR), heterotrophic feeding rates (stable isotope tracing of ¹³C‑POM into coral tissue), and microbiome composition (16S rRNA gene sequencing, metagenomics for enzyme genes).
• Apply calmodulin inhibitor (W‑7) in a subset to test dependency on Ca²⁺‑binding proteins.
• Statistical analysis via mixed‑effects models to test interaction effects of stressors, feeding treatment, and microbial shifts on calcification.

If predictions hold, the hypothesis establishes a mechanistic link between ion transporter dysfunction, heterotrophic plasticity, and microbiome-mediated nutrient recycling as a determinant of coral resilience under multi‑stressor scenarios. Failure to observe the predicted interactions would falsify the proposed feedback, indicating that other pathways dominate the coral response to OA and heat.