Hypothesis

We propose that coral colonies maintain a spatial telomere gradient: polyps at the growth front express high telomerase activity and robust DNA‑repair pathways, protecting host genomic integrity, while older polyps toward the colony periphery experience progressive telomere erosion and rely on apoptosis or senescence to remove damaged cells. Ocean acidification disrupts this gradient by elevating intracellular ROS/RNS, depleting Symbiodinium‑derived antioxidants, and accelerating telomere damage specifically at the growth front. When telomere dysfunction exceeds a threshold, the protective somatic ‘quasi‑germline’ layer fails, regenerative budding collapses, and the colony shifts to a net‑loss state.

Mechanistic Rationale

1. Telomerase localization – In many stem‑cell systems, telomerase activity is confined to a niche that sustains proliferative capacity. We hypothesize that coral growth‑front polyps constitute such a niche, showing detectable TERT transcript and protein levels, whereas basal polyps show minimal expression.
2. Antioxidant buffering – Symbiodinium provide superoxide dismutase and catalase that scavenge acidification‑induced ROS at the tissue surface. Loss of these symbionts (observed at pH 7.6–7.8) removes a critical shield, allowing peroxynitrite to oxidize telomeric guanine residues, triggering telomere uncapping.
3. Damage clearance – Peripheral polyps, already experiencing telomere attrition, activate p53‑dependent apoptosis when ROS levels rise, effectively culling damaged units. This mirrors germline‑like selection pressure but operates in a somatic context.
4. Feedback loop – As growth‑front telomerase declines under oxidative stress, fewer new polyps are generated, reducing the colony’s capacity to dilute damage via budding, creating a positive feedback toward senescence.

Testable Predictions

• Spatial telomere length – Quantitative FISH or qPCR on microdissected growth‑front vs. peripheral polyps will show significantly longer telomeres in the front under ambient pH (8.1) but not under low pH (7.7).
• Telomerase activity – TRAP assays will reveal high telomerase activity in growth‑front polyps at pH 8.1, dropping >50% after 7 days at pH 7.7; peripheral polyps will remain low in both conditions.
• ROS and symbiont density – ROS probes (e.g., DHE) will co‑localize with telomere damage markers (γ‑H2AX, 8‑oxoG) in growth‑front polyps under acidification only when Symbiodinium density falls below 30% of control.
• Functional rescue – Exogenous addition of the antioxidant mito‑TEMPO or transfection of TERT mRNA into growth‑front polyps under low pH will preserve telomere length, maintain budding rates, and reduce peripheral apoptosis compared with untreated controls.
• Allelic signature – Colonies that survive long‑term acidification will show enrichment of alleles associated with higher telomerase promoter activity or antioxidant enzyme variants, detectable via pooled‑seq of recruited juveniles.

Falsification

If telomere length shows no consistent front‑to‑periphery difference, or if telomerase activity remains uniformly low across all polyps regardless of pH, the core assumption of a protected somatic ‘quasi‑germline’ layer is invalid. Likewise, if antioxidant supplementation fails to rescue telomere integrity or budding under acidification, the proposed ROS‑mediated mechanism would be refuted.

Broader Implication

Demonstrating a germline‑like somatic strategy in corals would reframe ideas about metagenomic longevity, suggesting that engineering telomere maintenance in selected somatic lineages could enhance resilience of other modular organisms facing environmental stress.