Tropical stony corals host diverse microbial nitrogen dynamics

Abstract

Coral health hinges on an intricate relationship between the coral animal, photosynthetic algae of the family Symbiodiniaceae, and a microbial community of bacterial, archaeal, fungal, and viral associates collectively termed the coral holobiont. This holobiont maintains the nutrient balance of their symbiosis amid reefs’ otherwise oligotrophic environment, including by cycling physiologically important nitrogen compounds. Nitrogen (N) fixation has been well quantified in corals in accounting for the source of their fixed N, but no complementary loss term had been directly detected. This pathway is important for understanding sources and sinks of nitrogen on reefs and how they may impact coral success. Here we use 15N-tracer experiments to produce the first measurements of nitrate reduction, nitrite oxidation, and nitrous oxide (N2O) production in five species of reef-building corals in the Gardens of the Queen, Cuba. Nitrate reduction and nitrite oxidation are present in most species sampled, but ammonium oxidation is low potentially due to photoinhibition and competition with uptake. Coral-associated rates of N2O production indicate potential for denitrification, although there are variations among species. The brain coral Diploria labyrinthiformis exhibits the strongest potential for denitrification based on elevated rates of nitrate reduction and N2O production. This is in contrast with the elkhorn coral, Acropora palmata, which hosts minimal active nitrogen metabolism directly. Species sampled at multiple sites (Porites porites and Orbicella faveolata) showed similar trends among replicates and within genera (Porites). We also examine the impact of light and dark treatments on coral-associated nitrogen cycling. We hypothesized that dark conditions would stimulate anoxia via decreased photosynthesis and, in turn, denitrification. Most species, including two of the genus Porites, display higher rates of nitrate reduction and nitrite oxidation in the dark. In contrast, the mountainous star coral Orbicella faveolata displays the highest rates of nitrate reduction and nitrite oxidation measured, but only under ambient light, implying at least partial mediation by phototrophic associates. These measurements directly confirm the potential of coral symbionts to conduct denitrifying metabolisms, which had previously been inferred by molecular evidence.