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

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 (N 2 ) 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 N 2 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 N 2 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.

Contrasting Microbiome Dynamics of Putative Denitrifying Bacteria in Two Octocoral Species Exposed to Dissolved Organic Carbon (DOC) and Warming

“…Microbial community compositions in coral holobionts are highly selective due to different host functional or life history traits pertaining to e.g., development, physiology, and metabolism ( 17 , 40 , 68 ). Due to a relatively low capacity to obtain (in)organic N sources from the surrounding environment, P. flava is likely to rely more on symbiotic N cycling microbes to acquire or remove N to fulfill its metabolic requirements ( 13 , 28 , 69 ).…”

“…In particular, denitrifiers, that is, prokaryotes that encompass the reduction of nitrate or nitrite to dinitrogen gas ( 27 ), might help alleviate excess N stress of holobionts ( 7 ). Denitrifiers appear to be widely associated with many reef organisms and their activity was recently confirmed in corals from the Red Sea ( 28 ). Specifically, it has been observed that the activity of microbial denitrification in coral holobionts increased with environmental N levels ( 29 ).…”

Anthropogenic nitrogen pollution threats and challenges to the health of South Asian coral reefs

“…The significance of the holobiont model for understanding coral nitrogen demand lies in the emerging, yet poorly understood, relationship between the community of microorganisms contributing to the holobiont and how nitrogen is cycled and regulated within corals (Glaze et al, 2022;Mohamed et al, 2022). Recent studies indicate that the holobiont microbial community may be key to regulating fluctuations in environmental nitrogen availability and in maintaining the critical relationship between the coral host and its endosymbionts (Tilstra et al, 2021). More precisely, the holobiont makeup may be important for stabilizing nitrogen availability and maintaining nitrogen limitation in the endosymbiont via the relative actions of denitrifying and nitrogen-fixing bacteria.…”

“…More precisely, the holobiont makeup may be important for stabilizing nitrogen availability and maintaining nitrogen limitation in the endosymbiont via the relative actions of denitrifying and nitrogen-fixing bacteria. Whilst nitrogen fixation has been reported as a critical process supporting primary production by zooxanthellae endosymbionts during periods of low nutrient availability (Rädecker et al, 2015), it has also been reported that regulation of nitrate availability by microbial denitrification rates can occur when ambient nitrate concentrations are high thus potentially limiting the zooxanthellae response to elevated nutrient levels (Tilstra et al, 2021). Yet despite nitrogen fixation by free-living and colonial pelagic diazotrophs (Bell, 1992;El-Khaled et al, 2020), by benthic organisms (Cardini et al, 2014) and by bacterial symbionts (Lesser et al, 2007) being common within reef environments, nitrogen fixation is currently considered to be only a minor to moderate source of fixed nitrogen in the overall coral nitrogen budget, with estimates generally indicating a supply of <10%, but perhaps reaching as high as 20% under certain specific conditions (Rädecker et al, 2015;Benavides et al, 2017;Glaze et al, 2022;Moynihan et al, 2022).…”