In situ eutrophication stimulates dinitrogen fixation, denitrification, and productivity in Red Sea coral reefs

Abstract

<jats:p>Eutrophication (i.e. the increase of [in-]organic nutrients) may affect the functioning of coral reefs, but knowledge about the effects on nitrogen (N) cycling and its relationship to productivity within benthic reef communities is scarce. Thus, we investigated how <jats:italic>in situ</jats:italic> manipulated eutrophication impacted productivity along with 2 counteracting N-cycling pathways (dinitrogen [N<jats:sub>2</jats:sub>]-fixation, denitrification), using a combined acetylene assay. We hypothesised that N<jats:sub>2</jats:sub>-fixation would decrease and denitrification increase in response to eutrophication. N fluxes and productivity (measured as dark and light oxygen fluxes assessed in incubation experiments) were determined for 3 dominant coral reef functional groups (reef sediments, turf algae, and the scleractinian coral <jats:italic>Pocillopora verrucosa</jats:italic>) after 8 wk of <jats:italic>in situ</jats:italic> nutrient enrichment in the central Red Sea. Using slow-release fertiliser, we increased the dissolved inorganic N concentration by up to 7-fold compared to ambient concentrations. Experimental nutrient enrichment stimulated both N<jats:sub>2</jats:sub>-fixation and denitrification across all functional groups 2- to 7-fold and 2- to 4-fold, respectively. Productivity doubled in reef sediments and remained stable for turf algae and <jats:italic>P. verrucosa</jats:italic>. Our data therefore suggest that (1) turf algae are major N<jats:sub>2</jats:sub>-fixers in coral reefs, while denitrification is widespread among all investigated groups; (2) surprisingly, and contrary to our hypothesis, both N<jats:sub>2</jats:sub>-fixation and denitrification are involved in the response to moderate N eutrophication, and (3) stimulated N<jats:sub>2</jats:sub>-fixation and denitrification are not directly influenced by productivity. Our findings underline the importance and ubiquity of microbial N cycling in (Red Sea) coral reefs along with its sensitivity to eutrophication.</jats:p>

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

“…Incredibly, the nitrate reduction rates observed here are on par with those observed in the anoxic marine oxygen minimum zones that are characterized by their hosting the denitrification metabolism [ 87 , 88 ]. Indeed, evidence is emerging that denitrification is also important among analogous Red Sea corals [ 89 , 90 ] The ability of natural coral-associated communities to reduce nitrate and denitrify is especially important to buffer against negative impacts in the Anthropocene, when increasing nitrogen supply can increase severity of coral disease [ 3 , 4 ] and bleaching altogether [ 91 ].…”

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

“…Briefly, COBRA incubations were performed in gastight 1 L glass chambers (800 mL seawater + 200 mL headspace). As acetylene inhibits the production of NO 3 - via nitrification 141 , 142 , seawater (ambient NO 3 - concentrations ranged between 0.09 and 0.34 µM) 21 , 112 was supplemented with nitrate to a final concentration of 5 µM as a substrate for the denitrification pathway to counteract substrate limitation (see supplementary material SM 5 ). Incubations with nitrate amended seawater have been performed successfully in previous studies 141 – 145 .…”

“…Likewise, fixed N can be transformed into atmospheric N 2 via anaerobic ammonium oxidation (ANAMMOX), a pathway functioning as an additional N removing mechanism in coral reef sponges 15 , and hypothetically in other coral reef associated organisms 12 . Whereas N influxes to coral reefs via N 2 fixation are comparably well-studied 10 , 16 , 17 , knowledge about N efflux via denitrification is limited to some coral reef substrates (such as reef sediments) 13 , 14 , and is just starting to be generated for other coral reef organisms (e.g., hard corals) 18 – 21 . Corals reefs and their main ecosystem engineers, scleractinian corals, are adapted to nutrient-poor environments 22 , 23 .…”

Relative abundance of nitrogen cycling microbes in coral holobionts reflects environmental nitrate availability

“…On the other hand, microbes capable of denitrification, i.e. the chemical reduction of nitrate to N 2 , may play a putative role in alleviating the coral holobiont from excess N [ 21 , 22 ]. It was hypothesized that high denitrification rates may maintain N limitation for Symbiodiniaceae, and, as a result, may potentially support the functioning of the coral–Symbiodiniaceae symbiosis [ 9 , 11 ].…”

“…Making use of the pronounced seasonality of the central Red Sea, the present study aimed to (i) assess patterns in the abundance of denitrifiers (approximated via nirS gene copy numbers) in relation to diazotrophs (approximated via nifH gene copy numbers) in a seasonal resolution (herein referred to as nirS to nifH gene abundance ratios); and (ii) identify environmental parameters potentially driving the observed seasonal patterns. Due to the potential stimulating or suppressing effects of dissolved inorganic N (DIN) on denitrification [ 22 , 25 ] and diazotrophy [ 22 , 26 – 29 ], respectively, we hypothesized that the seasonal patterns of nirS to nifH gene abundance ratios in coral holobionts would be mostly affected by DIN, i.e. nitrate, nitrite and/or ammonium concentrations.…”