The aging program of the coral holobiont is governed not by host nuclear or mitochondrial DNA but by the mitochondrial genome of its Symbiodiniaceae symbionts. Subtle variation in symbiont mtDNA alters electron transport chain efficiency, modulating reactive oxygen species (ROS) output that acts as a retrograde signal to the host nucleus. This ROS signal reshapes host gene networks governing apoptosis, autophagy, and immune activation, thereby setting the pace of holobiont senescence and bleaching susceptibility. In essence, symbiont mtDNA functions as a metabolic rheostat that translates environmental stress into host‑level aging outcomes.

Mechanistically, differences in symbiont mtDNA-encoded subunits of cytochrome b and COX1 change the proton‑pumping capacity of the symbiont respiratory chain. Higher ROS production triggers host MAPK and NF‑κB pathways, upregulating caspases and lysosomal enzymes that accelerate cellular turnover. Conversely, low‑ROS haplotypes sustain a more reduced state, promoting host antioxidant gene expression (e.g., superoxide dismutase, glutathione peroxidase) and delaying apoptosis. This creates a feedback loop where host‑derived nitric oxide can further modulate symbiont mitochondrial membrane potential, fine‑tuning ROS emission.

Testable predictions:

1. Isogenic Symbiodiniaceae lines differing only at a single mtDNA heteroplasmic site (e.g., a synonymous mutation in COX1) will produce measurable ROS gradients under identical light and temperature conditions.
2. Exposing aposymbiotic Acropora juveniles to these lines will yield divergent host transcriptomic profiles: high‑ROS lines will elevate expression of caspase‑3, bax, and hsp70, while low‑ROS lines will upregulate sod2, foxO, and lon protease.
3. Chronic thermal stress (32 °C for 7 days) will shorten the holobiont lifespan (measured by survival and fecundity) in high‑ROS symbiont associations by ≥30 % compared with low‑ROS associations, independent of symbiont density.
4. Targeted reduction of symbiont mtDNA mutation load using mitoTALENs to shift heteroplasmy toward low‑ROS haplotypes will rescue host longevity and reduce bleaching incidence under stress.

Falsifiability: If manipulation of symbiont mtDNA heteroplasmy fails to alter host ROS signaling, gene expression, or stress‑induced lifespan, or if host longevity remains tightly coupled to host mtDNA mutation load regardless of symbiont genotype, the hypothesis is refuted. This approach shifts focus from the host genome to the symbiont mitochondrion as a tractable, editable locus for enhancing coral resilience.