Denitrification Aligns with N2 Fixation in Red Sea Corals

Abstract

Denitrification may potentially alleviate excess nitrogen (N) availability in coral holobionts to maintain a favourable N to phosphorous ratio in the coral tissue. However, little is known about the abundance and activity of denitrifiers in the coral holobiont. The present study used the nirS marker gene as a proxy for denitrification potential along with measurements of denitrification rates in a comparative coral taxonomic framework from the Red Sea: Acropora hemprichii, Millepora dichotoma, and Pleuractis granulosa. Relative nirS gene copy numbers associated with the tissues of these common corals were assessed and compared with denitrification rates on the holobiont level. In addition, dinitrogen (N2) fixation rates, Symbiodiniaceae cell density, and oxygen evolution were assessed to provide an environmental context for denitrification. We found that relative abundances of the nirS gene were 16- and 17-fold higher in A. hemprichii compared to M. dichotoma and P. granulosa, respectively. In concordance, highest denitrification rates were measured in A. hemprichii, followed by M. dichotoma and P. granulosa. Denitrification rates were positively correlated with N2 fixation rates and Symbiodiniaceae cell densities. Our results suggest that denitrification may counterbalance the N input from N2 fixation in the coral holobiont, and we hypothesize that these processes may be limited by photosynthates released by the Symbiodiniaceae.

Simultaneous Measurements of Dinitrogen Fixation and Denitrification Associated With Coral Reef Substrates: Advantages and Limitations of a Combined Acetylene Assay

“…The simultaneous presence of these antinomic processes has been detected in coral reef associated sediments (Koop et al, 2001) and microbial mats (Joye and Paerl, 1993) before. Potentially, both pathways can be carried out by the same microbes (Bothe et al, 1981) and are indirectly linked by their similar environmental requirements (Tilstra et al, 2019). Absolute N 2 -fix rates (i.e., calculated based on sampling points t 0 and t 12 ) measured in the present study were in the same range for turf algae (Rix et al, 2015) and coral rubble (Cardini et al, 2016), who also obtained N 2 -fix rates via acetylene-based assays (Table 2).…”

Trait-Based Comparison of Coral and Sponge Microbiomes

“…Furthermore, it is likely that some anaerobic metabolism could occur in the coral microbiome at night due to diurnal fluctuations in tissue pO 2 . However, spatial separation can also allow for simultaneous aerobic and anaerobic processes and pO2 was not found to influence denitrification and nitrogen fixation rates in Red Sea stony coral 71 . Dissimilatory metabolism thus appears to represent a mix of potential convergence (e.g., lack of significant differences based on short-read analysis) and some specialization (i.e., DNRA in X. muta) between host species.…”

“…Denitrification was also not detected in either host species. Dentrifying bacteria have been observed in coral 72,74 and recently, denitrification rates were documented for three coral species in the Red Sea 71 . Thus, either denitrification does not occur in this coral, M. cavernosa, or it was not occurring at the time of sampling.…”

“…Ultimately, the use of multiple approaches (short read analysis, assembly analysis, and metagenome prediction) to compare the functional profiles of M. cavernosa and X. muta uncovered two key results: (1) similar to other studies, the overlap in functional profiles between the metatranscriptome and the metagenome predictions was relatively high (Table 2), providing support for these metagenome prediction programs in future work, and (2) we observed indications of both convergence and specialization within the host microbiomes. www.nature.com/scientificreports www.nature.com/scientificreports/ coral-microbe symbioses 18,53,70,71 . In the current study, there was often overlap in the presence of major pathways for nutrient acquisition and/or catabolism, with only a few specific pathways (i.e., DNRA, sulfur oxidation) exclusive to sponges or corals.…”

Holobiont Nitrogen Control and its Potential for Eutrophication Resistance in an Obligate Photosymbiotic Jellyfish

“…The host benefits from a limited N availability [8,20] as excess inorganic N can disrupt the host-symbiont partnership by altering the N to phosphate ratio within the holobiont and exacerbate heat-induced bleaching [17,21]. Recently, prokaryote associates have also been linked to contribute to Symbiodiniaceae N limitation in coral holobionts by metabolizing and therefore limiting biologically available N [18,22].…”