Coral reef health depends on an intricate relationship among the coral animal, photosynthetic algae, and a complex microbial community. The holobiont can impact the nutrient balance of their hosts amid an otherwise oligotrophic environment, including by cycling physiologically important nitrogen compounds. Here we use 15N-tracer experiments to produce the first simultaneous measurements of ammonium oxidation, nitrate reduction, and nitrous oxide (N2O) production among five iconic species of reef-building corals (Acropora palmata, Diploria labyrinthiformis, Orbicella faveolata, Porites astreoides, and Porites porites) in the highly protected Jardines de la Reina reefs of Cuba. Nitrate reduction is present in most species, but ammonium oxidation is low potentially due to photoinhibition and assimilatory competition. Coral-associated rates of N2O production indicate a widespread potential for denitrification, especially among D. labyrinthiformis, at rates of ~1 nmol cm-2 d-1. In contrast, A. palmata displays minimal active nitrogen metabolism. Enhanced rates of nitrate reduction and N2O production are observed coincident with dark net respiration periods. Genomes of bacterial cultures isolated from multiple coral species confirm that microorganisms with the ability to respire nitrate anaerobically to either dinitrogen gas or ammonium exist within the holobiont. This confirmation of anaerobic nitrogen metabolisms by coral-associated microorganisms sheds new light on coral and reef productivity.

There are a few baseline reef-systems available for understanding the microbiology of healthy coral reefs and their surrounding seawater. Here, we examined the seawater microbial ecology of 25 Northern Caribbean reefs varying in human impact and protection in Cuba and the Florida Keys, USA, by measuring nutrient concentrations, microbial abundances, and respiration rates as well as sequencing bacterial and archaeal amplicons and community functional genes. Overall, seawater microbial composition and biogeochemistry were influenced by reef location and hydrogeography. Seawater from the highly protected crown jewel offshore reefs in Jardines de la Reina, Cuba had low concentrations of nutrients and organic carbon, abundant Prochlorococcus, and high microbial community alpha diversity. Seawater from the less protected system of Los Canarreos, Cuba had elevated microbial community beta-diversity whereas waters from the most impacted nearshore reefs in the Florida Keys contained high organic carbon and nitrogen concentrations and potential microbial functions characteristic of microbialized reefs. Each reef system had distinct microbial signatures and within this context, we propose that the protection and offshore nature of Jardines de la Reina may preserve the oligotrophic paradigm and the metabolic dependence of the community on primary production by picocyanobacteria.