Decoding coral resistance to eutrophication through the association of hyper‑efficient denitrifiers as key microbial allies

Abstract

Abstract Coral reefs face a perilous future due to global climate change compounded by the increasing prevalence of local stressors. Prominent among these is nutrient pollution, particularly nitrate eutrophication, which disrupts the coral-algal symbiosis and escalates reef degradation. While microbial denitrification is hypothesized to mitigate nitrate stress, the mechanisms underlying coral resilience remain unknown. Studying Hong Kong’s coral “reef oases” that persist under chronic hyper-eutrophication, we discovered that resilience is not mediated by diversity or abundance shifts in denitrifier genera but by the association with specific, hyper-efficient denitrifying populations within the dominant denitrifier genus Ruegeria . By integrating population genomics, subspecies-resolution metabarcoding (resolving both the entire Ruegeria community and the denitrifying sub-community), and direct isotope-based activity assays, we identified and validated putative denitrifying “specialist” populations. These specialists were significantly enriched in corals from high-nitrate waters and exhibited 10-fold higher denitrification rates in low-oxygen incubations, converting nitrate to inert N 2 with superior efficiency compared to non-specialists. Our findings reveal that critical ecosystem-scale adaptations to anthropogenic change can occur through a unique association with specialized sub-genus populations, which may be missed in conventional microbiome surveys. As such, our work sheds light into why dominant denitrifying genera are ubiquitous, yet only certain corals thrive in eutrophic conditions. It also provides a framework for future studies delineating ecologically important host-associated microbes.