A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

Abstract

Assimilation of inorganic nitrogen from nutrient-poor tropical seas is an essential challenge for the endosymbiosis between reef-building corals and dinoflagellates. Despite the clear evidence that reef-building corals can use ammonium as inorganic nitrogen source, the dynamics and precise roles of host and symbionts in this fundamental process remain unclear. Here, we combine high spatial resolution ion microprobe imaging (NanoSIMS) and pulse-chase isotopic labeling in order to track the dynamics of ammonium incorporation within the intact symbiosis between the reefbuilding coral Acropora aspera and its dinoflagellate symbionts. We demonstrate that both dinoflagellate and animal cells have the capacity to rapidly fix nitrogen from seawater enriched in ammonium (in less than one hour). Further, by establishing the relative strengths of the capability to assimilate nitrogen for each cell compartment, we infer that dinoflagellate symbionts can fix 14 to 23 times more nitrogen than their coral host cells in response to a sudden pulse of ammoniumenriched seawater. Given the importance of nitrogen in cell maintenance, growth and functioning, the capability to fix ammonium from seawater into the symbiotic system may be a key component of coral nutrition. Interestingly, this metabolic response appears to be triggered rapidly by episodic nitrogen availability. The methods and results presented in this study open up for the exploration of dynamics and spatial patterns associated with metabolic activities and nutritional interactions in a multitude of organisms that live in symbiotic relationships.

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

“…Although corals have several ways to acquire nitrogen, either via heterotrophic feeding (Houlbrèque and Ferrier-Pagès, 2009) or via the uptake of inorganic nitrogen through their symbionts (Grover and Maguer, 2002;Pernice et al, 2012), nitrogen remains a recurrent limiting nutrient for the growth and health of corals (Béraud et al, 2013). Crossland and Barnes (1976) and Williams et al (1987) were the first to report N 2 fixation activity in the stony corals Acropora cuminata and Goniastrea australensis, and Acropora variabilis, respectively.…”

Symbiosis as a General Principle in Eukaryotic Evolution

“…Perhaps such a relationship is frequently confounded by microbe -microbe and microbehost interactions, resulting in spatiotemporal variation in the traits of microorganisms. Recent advances in single-cell imaging and single-cell sequencing (Pamp et al 2012;Pernice et al 2012;Lasken 2013) offer unprecedented opportunities to investigate such heterogeneity.…”

Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora

“…Support for this is provided by recent work that used NanoSIMS to demonstrate ammonium assimilation from 15 N-labelled ammonium ( 15 NH 4 Cl) in cells of both the coral host (that is, Acropora aspera and Isopora palifera) and Symbiodinium symbionts after just 1-h incubation (Pernice et al, 2012;Pernice et al, 2014). NanoSIMS technology has also been used to show the incorporation and translocation of labelled ammonium ( 15 NH 4 ) originating from nitrogen-enriched cultured bacteria (Vibrio sp.…”

“…Rapid uptake of ammonium by the coral animal and transfer to symbiotic dinoflagellates have been demonstrated through molecular studies (Yellowlees et al, 2008;Stambler, 2011) and hypothesized to be key strategies in the nutritional economy of cnidarians that have evolved in nutrient-poor waters (Pernice et al, 2012;Kopp et al, 2013). Support for this is provided by recent work that used NanoSIMS to demonstrate ammonium assimilation from 15 N-labelled ammonium ( 15 NH 4 Cl) in cells of both the coral host (that is, Acropora aspera and Isopora palifera) and Symbiodinium symbionts after just 1-h incubation (Pernice et al, 2012;Pernice et al, 2014).…”