Abstract
Recent research suggests that nitrogen (N) cycling microbes are important for coral holobiont functioning. In particular, coral holobionts may acquire bioavailable N via prokaryotic dinitrogen (N2) fixation or remove excess N via denitrification activity. However, our understanding of environmental drivers on these processes in hospite remains limited. Employing the strong seasonality of the central Red Sea, this study assessed the effects of environmental parameters on the proportional abundances of N cycling microbes associated with the hard corals Acropora hemprichii and Stylophora pistillata. Specifically, we quantified changes in the relative ratio between nirS and nifH gene copy numbers, as a proxy for seasonal shifts in denitrification and N2 fixation potential in corals, respectively. In addition, we assessed coral tissue-associated Symbiodiniaceae cell densities and monitored environmental parameters to provide a holobiont and environmental context, respectively. While ratios of nirS to nifH gene copy numbers varied between seasons, they revealed similar seasonal patterns in both coral species, with ratios closely following patterns in environmental nitrate availability. Symbiodiniaceae cell densities aligned with environmental nitrate availability, suggesting that the seasonal shifts in nirS to nifH gene abundance ratios were probably driven by nitrate availability in the coral holobiont. Thereby, our results suggest that N cycling in coral holobionts probably adjusts to environmental conditions by increasing and/or decreasing denitrification and N2 fixation potential according to environmental nitrate availability. Microbial N cycling may, thus, extenuate the effects of changes in environmental nitrate availability on coral holobionts to support the maintenance of the coral–Symbiodiniaceae symbiosis.
Highlights
The oligotrophic nature of coral reefs requires an efficient use and recycling of the available nutrients within the ecosystem, including by their main engineers, scleractinian corals
Due to the potential stimulating or suppressing effects of dissolved inorganic N (DIN) on denitrification [22,25] and diazotrophy [22,26,27,28,29], 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
To test for differences in nirS and nifH gene abundance ratios and Symbiodiniaceae cell densities between seasons, two-factorial univariate PERMANOVAs were performed with season and coral species as main factors based on Euclidian distances of square-root transformed data [39], while one-factorial univariate PERMANOVAs were performed with the season as the main factor for environmental parameters based on Euclidian distances of normalized data [39]
Summary
The oligotrophic nature of coral reefs requires an efficient use and recycling of the available nutrients within the ecosystem, including by their main engineers, scleractinian corals. This may include natural fluctuations, e.g. seasonality in N availability [13,14,15,16], as well as anthropogenic N inputs [17] In this sense, coral-associated microbes, in particular prokaryotes, may play an integral role in coral holobiont N cycling. 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] To this end, the presence of denitrifiers in coral holobionts was first reported in the late 2000s [23,24], but Tilstra et al [21] only recently demonstrated that denitrification constitutes an active metabolic pathway present in coral holobionts from the oligotrophic central Red Sea. Taken together, microbial N cycling contributes to N availability for the coral holobiont. Due to the potential stimulating or suppressing effects of dissolved inorganic N (DIN) on denitrification [22,25] and diazotrophy [22,26,27,28,29], 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
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