Discovery and quantification of anaerobic nitrogen metabolisms among oxygenated tropical Cuban stony corals

Andrew R Babbin,Maickel Armenteros,María Victoria Iglesias Rodríguez,Amy Apprill,Diana Dumit,Scott D Wankel,Sarah L Schwartz,Tyler Tamasi,Laura Weber

doi:10.1038/s41396-020-00845-2

Abstract

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.

Highlights

Corals reefs are critical environments hosting diverse marine life despite a confined footprint within Earth’s oceanic extent [1]
Inorganic nitrogen concentrations were low throughout the sites, with ammonium and nitrate each
Separate shipboard nitrogen tracer experiments with P. astreoides, P. porites, D. labyrinthiformis, A. palmata, and O. faveolata showed that coral-associated nitrate reduction to nitrite were detected in all coral species, and ammonium oxidation was detected in all species except A. palmata (Fig. 3, Supplementary Table 2)

Summary

Introduction

Corals reefs are critical environments hosting diverse marine life despite a confined footprint within Earth’s oceanic extent [1]. They thrive in shallow waters within a broadband from 30° S to 30° N of warm, sunlit, and relatively oligotrophic ocean waters [2]. The health of the coral-algal partnership depends on a complex microbial community of bacterial, archaeal, fungal, and viral associates, collectively termed the coral holobiont [7] This holobiont maintains a delicate nutrient balance in order to support life among a reefs’ otherwise generally oligotrophic surroundings [8, 9]. One such nutrient, fixed nitrogen, is essential for the production of amino and nucleic acids and is a principal limiter of ocean productivity

Methods

Results

Conclusion