Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species

Valentine Meunier,Valentine Meunier,Andreas Ravache,Olivier Grosso,Olivier Grosso,Olivier Grosso,Olivier Grosso,Fanny Houlbrèque,Fanny Houlbrèque,Mar Benavides,Mar Benavides,Mar Benavides,Mar Benavides,Christophe Lambert,Christophe Lambert,Christophe Lambert,Christophe Lambert,Christophe Lambert,Sophie Bonnet,Sophie Bonnet,Sophie Bonnet,Sophie Bonnet

doi:10.3389/fmars.2021.692248

Abstract

Reef-building corals generally thrive in nutrient-poor tropical waters, where among other elements, nitrogen (N) availability often limits primary productivity. In addition to their close association with endosymbiotic dinoflagellates of the family Symbiodiniaceae, enabling an effective use and retention of dissolved inorganic nitrogen (DIN), scleractinian corals have developed strategies to acquire new N: (1) They can ingest N-rich sediment particles and preys (from picoplankton to macro-zooplankton) via heterotrophy, including diazotrophs [plankton fixing dinitrogen (N2) and releasing part of this nitrogen—Diazotroph-Derived N (DDN)—in seawater], a pathway called “heterotrophic nutrition on diazotrophs”; (2) Symbiotic diazotrophs located in the coral holobiont have the molecular machinery to fix N2, a pathway called “symbiotic N2 fixation”. Here we used the 15N2 isotopic labeling in a series of incubations to investigate the relative contribution of each of these DDN transfer pathways in three worldwide distributed coral species: Acropora muricata, Galaxea fascicularis, and Pocillopora damicornis. We show that N provision via “symbiotic N2 fixation” is negligible compared to that obtained via “heterotrophic nutrition on diazotrophs,” with DDN assimilation rates about a thousand times lower for P. damicornis and G. fascicularis, or assimilation rates via “symbiotic N2 fixation” almost nil for A. muricata. Through heterotrophic feeding on planktonic diazotrophs, only G. fascicularis and P. damicornis can successfully obtain N and fulfill a large part of their N requirements (DDN asimilation rates: 0.111 ± 0.056 and 0.517 ± 0.070 μg N cm–2 h–1 in their Symbiodiniaceae, respectively). Whereas this contribution is again negligible for A. muricata. They also largely consume the picoplankton that likely benefit from this DDN (Prochlorococcus and Synechococcus cells; respectively, 2.56 ± 1.57 104 and 2.70 ± 1.66 104 cell h–1 cm–2 for G. fascicularis; 3.02 ± 0.19 105 and 1.14 ± 0.79 104 cell h–1 cm–2 for P. damicornis). The present study confirms the different dependencies of the three tested species regarding heterotrophy, with P. damicornis and G. fascicularis appearing highly efficient at capturing plankton, while A. muricata, considered as mainly autotroph, does not rely on these food resources to meet its N and energy needs.

Highlights

Reef-building corals generally thrive in nutrient-poor tropical waters, where among others, nitrogen (N) availability often limits primary production (Howarth, 1988)
The present study investigated the patterns of Derived N (DDN) acquisition in three different coral species and allowed us, among other things, to identify whether these patterns changed according to their dependence on heterotrophy
P. damicornis and G. fascicularis appear to be highly efficient at capturing plankton, while A. muricata does not rely on these food resources to meet its N and energy needs

Summary

Introduction

Reef-building corals generally thrive in nutrient-poor tropical waters, where among others, nitrogen (N) availability often limits primary production (Howarth, 1988). Diazotrophs (dinitrogen (N2)fixing prokaryotes), are abundant in coral lagoon waters (Turk-Kubo et al, 2015; Messer et al, 2017; Saulia et al, 2020), and heterotrophic nutrition on diazotrophs represent a potential source of N for corals (Benavides et al, 2016; Meunier et al, 2019) This plankton fixes N2 (Tilstra et al, 2018) transform it into a bioavailable N form (NH4+), and releases part of the recently fixed N (Diazotroph-Derived N, DDN) in seawater, providing available N for the development of the planktonic food web (Berthelot et al, 2016; Bonnet et al, 2016). While recent works have shown that N acquisition through symbiotic N2 fixation greatly varies in relation to environmental factors, species, and corals’ metabolic status (Rädecker et al, 2015; Bednarz et al, 2017; Benavides et al, 2017; Lesser et al, 2018, 2019), heterotrophic nutrition on diazotrophs has only been demonstrated for one coral species, Stylophora pistillata in Benavides et al (2016) and Meunier et al (2019)

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