Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species
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 rete...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-07-01
|
| Series: | Frontiers in Marine Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2021.692248/full |
| _version_ | 1818457055481036800 |
|---|---|
| author | Valentine Meunier Sophie Bonnet Mar Benavides Andreas Ravache Olivier Grosso Christophe Lambert Fanny Houlbrèque |
| author_facet | Valentine Meunier Sophie Bonnet Mar Benavides Andreas Ravache Olivier Grosso Christophe Lambert Fanny Houlbrèque |
| author_sort | Valentine Meunier |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-14T22:36:29Z |
| format | Article |
| id | doaj.art-cbf4ec5256a241389d1214d28779521e |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-12-14T22:36:29Z |
| publishDate | 2021-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-cbf4ec5256a241389d1214d28779521e2022-12-21T22:45:08ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452021-07-01810.3389/fmars.2021.692248692248Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral SpeciesValentine Meunier0Sophie Bonnet1Mar Benavides2Andreas Ravache3Olivier Grosso4Christophe Lambert5Fanny Houlbrèque6Centre IRD Nouméa, UMR ENTROPIE (IRD, Université de La Réunion, CNRS, Université de La Nouvelle-Calédonie, Ifremer), Nouméa, New CaledoniaAix-Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, FranceAix-Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, FranceCentre IRD Nouméa, UMR ENTROPIE (IRD, Université de La Réunion, CNRS, Université de La Nouvelle-Calédonie, Ifremer), Nouméa, New CaledoniaAix-Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, FranceUniv Brest, CNRS, IRD, Ifremer, LEMAR, Plouzané, FranceCentre IRD Nouméa, UMR ENTROPIE (IRD, Université de La Réunion, CNRS, Université de La Nouvelle-Calédonie, Ifremer), Nouméa, New CaledoniaReef-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.https://www.frontiersin.org/articles/10.3389/fmars.2021.692248/fulldinitrogen fixationDDN assimilationscleractinian coralsheterotrophydiazotrophspicoplankton |
| spellingShingle | Valentine Meunier Sophie Bonnet Mar Benavides Andreas Ravache Olivier Grosso Christophe Lambert Fanny Houlbrèque Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species Frontiers in Marine Science dinitrogen fixation DDN assimilation scleractinian corals heterotrophy diazotrophs picoplankton |
| title | Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species |
| title_full | Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species |
| title_fullStr | Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species |
| title_full_unstemmed | Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species |
| title_short | Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species |
| title_sort | diazotroph derived nitrogen assimilation strategies differ by scleractinian coral species |
| topic | dinitrogen fixation DDN assimilation scleractinian corals heterotrophy diazotrophs picoplankton |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2021.692248/full |
| work_keys_str_mv | AT valentinemeunier diazotrophderivednitrogenassimilationstrategiesdifferbyscleractiniancoralspecies AT sophiebonnet diazotrophderivednitrogenassimilationstrategiesdifferbyscleractiniancoralspecies AT marbenavides diazotrophderivednitrogenassimilationstrategiesdifferbyscleractiniancoralspecies AT andreasravache diazotrophderivednitrogenassimilationstrategiesdifferbyscleractiniancoralspecies AT oliviergrosso diazotrophderivednitrogenassimilationstrategiesdifferbyscleractiniancoralspecies AT christophelambert diazotrophderivednitrogenassimilationstrategiesdifferbyscleractiniancoralspecies AT fannyhoulbreque diazotrophderivednitrogenassimilationstrategiesdifferbyscleractiniancoralspecies |