Reef-building corals farm and feed on their photosynthetic symbionts

Symbiotic reef-building corals are mixotrophs: their dinoflagellate symbionts can meet most or all of the host’s energetic carbon demand by translocating carbon-rich photosynthates. Yet, host growth and reproduction require nitrogen (N) and phosphorus (P), whose acquisition pathways are less clear. Corals are thought to obtain much of their N and P heterotrophically (particulate/dissolved organic matter), while symbionts recycle host metabolic N and P to promote their own growth and retain nutrients within the partnership. Coral animals can directly incorporate some ammonium, but this is quantitatively minor compared with substantially higher N assimilation by symbionts; corals lack the enzymes to assimilate nitrate, so NO3− and dissolved inorganic phosphate uptake occurs via the symbionts. Prior work has indicated N transfer from symbionts to hosts (e.g., amino acids, NanoSIMS visualization, in situ observations), but there has been no evidence for P transfer, and symbionts are often considered a P sink. Consequently, previously reported benefits of dissolved inorganic N and P for coral growth lacked a mechanistic basis. This study asks whether symbiont uptake of dissolved inorganic N and P can sustain host growth and whether corals obtain these nutrients by farming and digesting excess symbiont cells, and tests ecosystem-level implications where dissolved inorganic nutrients vary naturally.

Background literature cited in the text highlights: (1) Carbon transfer from symbionts can meet host energy needs but does not directly supply N and P needed for growth; (2) Coral hosts acquire N and P via heterotrophy and dissolved organic compounds, with symbionts recycling host wastes; (3) Host ammonium uptake is minor relative to symbiont N assimilation, and nitrate assimilation is exclusively via symbionts due to missing host enzymes; (4) Multiple studies show N transfer from symbionts to hosts (e.g., amino acid release, NanoSIMS, field observations), and that host amino acids can originate from symbionts; (5) No prior evidence supports P transfer from symbionts to hosts, with symbionts often viewed as a P sink; (6) Despite these gaps, experimental and field studies have reported that dissolved inorganic N and P can enhance coral growth, indicating an unresolved mechanism. These works frame the study’s focus on symbiont-mediated acquisition and host access to dissolved inorganic N and P.

Laboratory long-term experiments: The authors maintained multiple coral species in flow-through aquaria for more than 6.5 months under two nutrient regimes: nutrient-replete versus nutrient-limited concentrations of nitrate (NO3−) and phosphate (PO43−). Incoming seawater was UV-sterilized and microfiltered to remove particulate material that could serve as food, isolating dissolved inorganic N and P as nutrient sources assimilable by symbionts. Ten replicate colonies per treatment were used for each of nine host species in the main growth experiments. Growth metrics included changes in surface area, calcification (mass), and symbiont density over time. In nutrient-limited tanks, growth and calcification began to stagnate after around 50 days. Isotope pulse experiments quantified dissolved inorganic N uptake and partitioning. Corals received defined pulses of 15NO3− together with phosphate, and responses in surface area were compared with nutrient-replete controls. N uptake from water and net N gain by the holobiont (host tissue plus symbionts) were measured, with error estimates from independent samples collected on different days. Symbiont farming and digestion: The team estimated the proportion of the symbiont population digested by hosts (symbiont digestion ratio) by comparing expected symbiont population dynamics based on cell division (mitotic index, M+) and expulsion rates against observed symbiont abundances over time. Models reproducing observed changes required continuous removal of symbionts by the host. Correlations between the number of missing symbionts (relative to expected) and coral growth (area increase) were assessed under both nutrient-replete (203 days) and nutrient-limited (84 days) conditions across four species, with R2 and statistical significance reported. Natural experiment (field study): In the Chagos Archipelago (central equatorial Indian Ocean), islands vary in seabird densities and associated guano-derived nutrient inputs, creating a natural gradient in dissolved inorganic N supply and δ15N signatures. The δ15N of guano-derived dissolved inorganic N is high and serves as a tracer of symbiont-mediated N assimilation. The study measured δ15N in host tissues and symbionts of Acropora spp., along with potential N sources (zooplankton and a ‘fluid’ sample type) and macroalgae for comparison, from reefs adjacent to islands with high (+B) and low (−B) seabird densities. Statistical analyses included one-way ANOVA (p < 0.001) with Holm–Sidak post hoc tests, and linear regressions (adjusted R2 reported). Growth of Acropora colonies was measured as annual surface area expansion in a multi-year in situ tagging experiment across independent islands, with pairwise t-tests (two-tailed, p = 0.04). A geochemical mixing model using δ15N endmembers (guano and zooplankton) estimated the fraction of coral N derived from guano-sourced dissolved inorganic N via initial symbiont uptake.

• Symbiont-mediated uptake of dissolved inorganic N and P alone can sustain rapid coral growth in the absence of particulate food. Corals exposed to defined pulses of 15NO3− and phosphate showed increased surface area relative to nutrient-replete controls, indicating efficient utilization of dissolved nutrients via symbionts.
• In nutrient-limited aquaria without particulate food, growth and calcification slowed or stagnated after approximately 50 days, underscoring the dependence on nutrient availability.
• Modeling of symbiont population dynamics revealed that observed symbiont abundances over months could only be reproduced by continuous host removal (digestion) of excess symbionts. The number of ‘missing’ symbionts (relative to expected from mitosis and expulsion) correlated with coral growth (area increase) under both nutrient-replete (203 days) and nutrient-limited (84 days) conditions across four species, with strong correlations (R2 reported; all correlations significant at P < 0.0001).
• Laboratory measurements showed that symbionts have 14–23× higher nitrogen assimilation rates than hosts, reinforcing that inorganic N entry is dominated by the symbiont pathway; hosts cannot assimilate nitrate directly.
• Field natural experiment: δ15N values of both host tissues and symbionts of Acropora spp. were significantly higher on reefs adjacent to seabird islands (+B) than on reefs with low seabird densities (−B), consistent with uptake of guano-derived dissolved inorganic N by symbionts and subsequent transfer to hosts (ANOVA p < 0.001; Holm–Sidak post hoc significant differences). Macroalgae δ15N values matched the elevated coral host values at +B sites, while zooplankton δ15N did not significantly differ between +B and −B sites, indicating a predominantly allochthonous dissolved inorganic N signal rather than increased trophic N via zooplankton.
• A δ15N mixing model estimated that around 50% of coral N derives from guano-sourced dissolved inorganic N, entering via initial symbiont assimilation; heterotrophic acquisition (e.g., zooplankton feeding) contributed less than half to the host N budget under these conditions.
• Growth at ecosystem scale: Acropora colonies exhibited approximately twofold higher annual surface area expansion near high seabird-density islands compared to low-density islands (t-test, two-tailed p = 0.04), consistent with enhanced growth where dissolved inorganic N availability is elevated.
• Conceptual advance: Corals actively ‘farm’ their symbionts and feed on them to access dissolved inorganic N and P pools that are otherwise inaccessible to animal hosts, enabling corals to function effectively as autotrophs for C, N, and P when dissolved inorganic nutrients are sufficient.

The study resolves a central mechanistic gap in coral reef ecology by demonstrating that dissolved inorganic N and P assimilated by algal symbionts can be transferred to coral hosts through host digestion of excess symbiont cells. This mechanism—symbiont farming and feeding—explains how corals in oligotrophic waters can meet their N and P requirements, not solely via heterotrophy, but by tapping into inorganic nutrient pools through their photosynthetic partners. Laboratory evidence shows that symbiont-dominated inorganic nutrient uptake supports rapid host growth and that hosts continuously prune symbiont populations, with the magnitude of symbiont removal closely tracking host growth. Field isotopic data from seabird-fertilized reefs confirm that dissolved inorganic N assimilated by symbionts accounts for a substantial fraction (∼50%) of the coral N budget and is associated with higher coral growth at the ecosystem scale. Together, these findings reconcile previous observations of growth benefits from inorganic nutrient enrichment with a clear biological pathway and underscore the competitive advantage of coral-algal symbioses in accessing both inorganic and organic nutrient pools. The work also clarifies how nutrient regimes modulate resilience: sufficient dissolved inorganic N and P enable sustained growth via symbiont farming, whereas scarcity can lead to depletion of symbiont stocks, bleaching, and potential mortality, especially under compounding thermal stress.

This study reveals that reef-building corals can farm and feed on their photosynthetic symbionts to obtain essential N and P from dissolved inorganic sources, enabling sustained growth in oligotrophic environments. By quantifying symbiont-mediated nutrient acquisition, host digestion of symbionts, and ecosystem-scale isotope and growth patterns, the work provides a parsimonious mechanism linking dissolved inorganic nutrient availability to coral performance. These insights help explain coral ecological success and refine our understanding of coral nutrient budgets. Future research should: (1) quantify species-specific thresholds and kinetics for dissolved inorganic N and P uptake and symbiont digestion; (2) integrate thermal stress and light variability to model trade-offs between symbiont retention, bleaching risk, and nutrient acquisition; (3) resolve phosphorus dynamics and host assimilation pathways during symbiont digestion; and (4) assess how changing ocean stratification and anthropogenic nutrient inputs will differentially affect reef communities via this mechanism.