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

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.

Community structure of coral microbiomes is dependent on host morphology

“…Bacterial taxa involved in other steps of the nitrogen cycle (i.e., nitrification and denitrification) are also more common in those coral species that harbor potential diazotrophs. Several of these taxa that can conduct either, or both, nitrification and denitrification include members of the genus Vibrio, Marinobacter, and Pseudoaltermonas [15,91]. Among the microbiomes of the coral species examined here, members of the genus Endozoicomonas varied in abundance with respect to coral species and traits more than any other microbial genus.…”

“…In addition to freeliving diazotrophs, several important members of the reef community (i.e., corals and sponges) have the capability to fix nitrogen through symbiotic associations with diazotrophs [32,87,88]. It is well-known that the microbiomes of scleractinian corals harbor diazotrophic symbionts [34,35,37,38,41,42], as well as other prokaryotes that mediate transformations of inorganic nitrogen in processes such as nitrification, denitrification, and the anaerobic oxidation of ammonium (ANAMMOX) [11,43,[89][90][91]. For all corals studied here, members of the bacterial phyla Fig.…”

The diversity and functional capacity of microbes associated with coastal phototrophs

“…We found that only the blades of P. scouleri harbored MAGs with both anaerobic and aerobic biosynthetic pathways for Vitamin B 12 , suggesting that the variable oxygen environment driven by host-metabolism creates diverse metabolic niches for associated microbes. Strong gradients in oxygen and metabolically diverse microbial metabolisms are present in a diversity of animal hosts such as corals and sponges as a result of host metabolism (74-76). Fluctuating oxygen microenvironments might also promote cross-feeding, where microbial taxa produce a metabolite that can be consumed by other taxa.…”

“…The copyright holder for this preprint this version posted January 7, 2022. ; https://doi.org/10.1101/2022.01.05.475171 doi: bioRxiv preprint result of host metabolism (74)(75)(76). Fluctuating oxygen microenvironments might also promote cross-feeding, where microbial taxa produce a metabolite that can be consumed by other taxa.…”

Nitrogen fixation and denitrification activity differ between coral- and algae-dominated Red Sea reefs

“…Potentially, observed denitrification potential differences among the hard coral species and Xenia sp. occurred due to their different capacity in releasing and producing mucus 96 , 97 , with thick mucus layers favouring high anaerobic potentials that might facilitate denitrification 96 . It has been demonstrated recently that soft coral mucus does not provide a favourable habitat for associated diazotrophs 97 , which in return could explain observed comparatively low N 2 fixation rates.…”