The Assimilation of Diazotroph-Derived Nitrogen by Scleractinian Corals Depends on Their Metabolic Status

Abstract

Tropical corals are associated with a diverse community of dinitrogen (N2)-fixing prokaryotes (diazotrophs) providing the coral an additional source of bioavailable nitrogen (N) in oligotrophic waters. The overall activity of these diazotrophs changes depending on the current environmental conditions, but to what extent it affects the assimilation of diazotroph-derived N (DDN) by corals is still unknown. Here, in a series of 15N2 tracer experiments, we directly quantified DDN assimilation by scleractinian corals from the Red Sea exposed to different environmental conditions. We show that DDN assimilation strongly varied with the corals’ metabolic status or with phosphate availability in the water. The very autotrophic shallow-water (~5 m) corals showed low or no DDN assimilation, which significantly increased under elevated phosphate availability (3 µM). Corals that depended more on heterotrophy (i.e., bleached and deep-water [~45 m] corals) assimilated significantly more DDN, which contributed up to 15% of the corals’ N demand (compared to 1% in shallow corals). Furthermore, we demonstrate that a substantial part of the DDN assimilated by deep corals was likely obtained from heterotrophic feeding on fixed N compounds and/or diazotrophic cells in the mucus. Conversely, in shallow corals, the net release of mucus, rich in organic carbon compounds, likely enhanced diazotroph abundance and activity and thereby the release of fixed N to the pelagic and benthic reef community. Overall, our results suggest that DDN assimilation by corals varies according to the environmental conditions and is likely linked to the capacity of the coral to acquire nutrients from seawater.

Diazotrophs: Overlooked Key Players within the Coral Symbiosis and Tropical Reef Ecosystems?

“…So far only few studies have provided evidence of the assimilation of DDN by corals either using the natural δ 15 N signature of corals or the 15 N 2 labeling technique (Lesser et al, 2007;Grover et al, 2014;Benavides et al, 2016;Bednarz et al, 2017). Grover et al (2014) did not detect DDN assimilation by the coral, while the other studies did, underlining that DDN assimilation by corals is not a straightforward process but can be very variable depending on the current environmental conditions and the associated diazotrophic community.…”

“…As such, it is the N:P proportion what triggers or inhibits N 2 fixation, rather than dissolved inorganic nitrogen concentrations per se (Knapp, 2012). N:P ratios have been poorly investigated in reefs, and to the best of our knowledge only two studies have assessed the importance of low vs. high N:P ratios on N 2 fixation by reef diazotrophs: while the addition of phosphorus did not increase N 2 fixation in the water column of the Gulf of Aqaba (Red Sea; Foster et al, 2009), it doubled in the same reef waters in the presence of coral mucus (i.e., organic matter release; Bednarz et al, 2017), which can be very rich in phosphate . This suggests that a combination of phosphorus and carbon-rich photosynthates are necessary to enhance N 2 fixation.…”

“…On the other hand, corals like Montastrea cavernosa can be observed with or without some diazotroph (cyanobacteria) symbionts (Lesser et al, 2004), which raises the question whether diazotrophs are only acquired by corals upon nitrogen stress situations. In addition, corals do not always profit from DDN, especially shallow corals which receive sufficient dissolved inorganic nitrogen from the ambient seawater (Grover et al, 2014;Bednarz et al, 2017). In summary, these observations raise the question whether diazotrophs are real coral symbionts or if they are only acquired upon nitrogen stress situations.…”

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

“…A recent study that investigated the effects of temperature, nutrient pollution and algal cover on the microbiomes of three coral species, however, found that temperature variation explained differences in microbial community structure over time better than other measured seasonal parameters (Zaneveld et al, 2016). In summer, A. muricata harbored a significantly higher abundance of several Cyanobacterium OTUs, which might play a role in providing new nitrogen to the coral holobiont (Bednarz et al, 2017), since many cyanobacteria are capable of fixing nitrogen (i.e., diazotrophs). Fixation of dinitrogen by these bacteria is an important functional process for corals thriving in oligotrophic tropical environments as they can provide up to 15% of new nitrogen to corals (Bednarz et al, 2017).…”

“…In summer, A. muricata harbored a significantly higher abundance of several Cyanobacterium OTUs, which might play a role in providing new nitrogen to the coral holobiont (Bednarz et al, 2017), since many cyanobacteria are capable of fixing nitrogen (i.e., diazotrophs). Fixation of dinitrogen by these bacteria is an important functional process for corals thriving in oligotrophic tropical environments as they can provide up to 15% of new nitrogen to corals (Bednarz et al, 2017). Increases in the abundance and diversity of nitrogen-fixing bacteria in coral tissue has been observed previously under elevated temperatures (Santos et al, 2014;Cardini et al, 2015Cardini et al, , 2016 and between winter and summer (Cai et al, 2018).…”