Symbiodiniaceae Are the First Site of Heterotrophic Nitrogen Assimilation in Reef-Building Corals

Martinez, Stephane; Grover, Renaud; Baker, David M.; Ferrier‐Pagés, Christine

doi:10.1128/mbio.01601-22

Cited by 12 publications

(17 citation statements)

References 55 publications

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“…N assimilation pathways in scleractinian corals is an active field of research, and the sampling design used here was not intended to address this issue. Coral N supply relies on two main pathways: PN (by feeding) that ultimately derives its N from dissolved N (Houlbrèque and Ferrier‐Pagès 2009) and dissolved N itself (i.e.,

{NH}_{4}^{+}

, urea, amino acids,

{NO}_{3}^{-}

), translocated from the symbiont to the host, by transfer of N‐bearing compounds (Martinez et al 2022) or by symbiont pruning (Boschma 1925; Wiedenmann et al 2023). On the reef flat and at the atoll rim, the relative similarity of

{normalδ}^{15} N - ({NO}_{3}^{-} + {NO}_{2}^{-})

, δ 15 N‐PN, and CS‐δ 15 N values do not allow the stable isotopes to clarify N assimilation pathways for Porites .…”

Section: Discussionmentioning

confidence: 99%

Tracing the fate of seabird‐derived nitrogen in a coral reef using nitrate and coral skeleton nitrogen isotopes

Choisnard,

Duprey,

Wald

et al. 2024

Limnology & Oceanography

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Seabirds transfer nutrients from the ocean to their nesting island, potentially altering nitrogen (N) cycling within adjacent terrestrial and marine ecosystems. Yet, the processes involved in seabird‐N transfer along the land–sea continuum remain elusive. Using δ15N and δ18O measurements of groundwater nitrate, we demonstrate the role of brackish groundwater located within a coral island's landmass as a major reservoir of nitrate (at millimolar levels). Nearly all of the total dissolved seabird‐derived N leaching into the groundwater (mostly ammonium and uric acid) is converted to nitrate by nitrification, as supported by the relatively low δ18O of the groundwater nitrate (3.97‰ ± 0.30‰). Comparison of nitrate δ15N and δ18O suggests that little denitrification takes place within the groundwater lens, implying that the high δ15N of groundwater nitrate (13.73‰ ± 0.05‰) derives from the high trophic position of seabirds and postdepositional processes that increase the δ15N of seabird excreta. Seawater and coral skeleton samples from a reef flat exposed to groundwater had higher δ15N values than at sites devoid of groundwater influence, indicating that the main source of N at the latter site was the Subtropical Upper Water, while the groundwater nitrate dominated the exposed reef flat N pool up to 200 m from shore. In addition, these results indicate that coral‐bound δ15N can detect seabird‐derived nitrate δ15N, raising opportunities to reconstruct historical seabird‐N inputs to coral reefs in relation to climatic and other changes, such as the introduction of invasive species.

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{NH}_{4}^{+}

, urea, amino acids,

{NO}_{3}^{-}

{normalδ}^{15} N - ({NO}_{3}^{-} + {NO}_{2}^{-})

, δ 15 N‐PN, and CS‐δ 15 N values do not allow the stable isotopes to clarify N assimilation pathways for Porites .…”

Section: Discussionmentioning

confidence: 99%

Tracing the fate of seabird‐derived nitrogen in a coral reef using nitrate and coral skeleton nitrogen isotopes

Choisnard,

Duprey,

Wald

et al. 2024

Limnology & Oceanography

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“…Likewise, the amino acid nitrogen isotope analysis showed a different nitrogen signature for symbionts based on orientation. Previous studies have shown that under short laboratory conditions, the symbionts are the first site of heterotrophic assimilation 62 . Since the coral host and symbiont are also known to share nutrients in both directions 62 it would be expected that the hosts and symbionts will reach a steady state where they have a similar signature, which was not the case for the shade-adapted corals.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies have shown that under short laboratory conditions, the symbionts are the first site of heterotrophic assimilation 62 . Since the coral host and symbiont are also known to share nutrients in both directions 62 it would be expected that the hosts and symbionts will reach a steady state where they have a similar signature, which was not the case for the shade-adapted corals. Hence, the different signatures between the host and symbionts for the shade-adapted corals suggest unequal sharing of resources, where the symbiont is receiving nutrients obtained from ingested prey by the host 63 , but also has an alternative nutrient source that is not being shared.…”

Section: Discussionmentioning

confidence: 99%

Irradiance driven trophic plasticity in the coral Madracis pharensis from the Eastern Mediterranean

Goodbody-Gringley,

Martinez,

Bellworthy

et al. 2024

Sci Rep

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The distribution of symbiotic scleractinian corals is driven, in part, by light availability, as host energy demands are partially met through translocation of photosynthate. Physiological plasticity in response to environmental conditions, such as light, enables the expansion of resilient phenotypes in the face of changing environmental conditions. Here we compared the physiology, morphology, and taxonomy of the host and endosymbionts of individual Madracis pharensis corals exposed to dramatically different light conditions based on colony orientation on the surface of a shipwreck at 30 m depth in the Bay of Haifa, Israel. We found significant differences in symbiont species consortia, photophysiology, and stable isotopes, suggesting that these corals can adjust multiple aspects of host and symbiont physiology in response to light availability. These results highlight the potential of corals to switch to a predominantly heterotrophic diet when light availability and/or symbiont densities are too low to sustain sufficient photosynthesis, which may provide resilience for corals in the face of climate change.

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“…However, interpretation of bulk tissue isotope values can sometimes be compromised by overlapping values between predators and potential food items and/or by the difficulty of sampling all possible food items. To address this issue, compound‐specific isotope analyses (CSIA) of fatty acids and amino acids have been successfully used in deep and shallow MAFs to investigate their food sources and to reveal variations in the heterotrophic contribution among conspecific organisms (Gori et al ., 2018; Fox et al ., 2019; Martinez et al ., 2022). The basic principle of CSIA is that some fatty acids and/or amino acids (AAs) are routed directly from the diet into the animal tissue, hence they remain unchanged, while others are biochemically transformed during assimilation.…”

Section: Tools To Assess Heterotrophy In Mafsmentioning

confidence: 99%

“…For instance, metals contained in plankton ingested by the coral host are absorbed by algal symbionts for photosynthesis (Ferrier‐Pagès, Sauzéat & Balter, 2018). Similarly, studies applying CSIA‐AA to nitrogen cycling in symbiotic corals have demonstrated that essential amino acids present in plankton prey are utilised by the algal symbionts instead of the host, although algae can synthesise essential amino acids (Martinez et al ., 2022). Therefore, further research is needed before isotope‐based inferences of heterotrophy can be made (e.g.…”

Section: Knowledge Gapsmentioning

confidence: 99%

Heterotrophy in marine animal forests in an era of climate change

Denis,

Ferrier‐Pagès,

Schubert

et al. 2024

Biological Reviews

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Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three‐dimensional structures formed by suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in the world's oceans. However, MAFs are in decline due to global and local stressors that threaten the survival and growth of their foundational species and associated biodiversity. Innovative and scalable interventions are needed to address the degradation of MAFs and increase their resilience under global change. Surprisingly, few studies have considered trophic interactions and heterotrophic feeding of MAF suspension feeders as an integral component of MAF conservation. Yet, trophic interactions are important for nutrient cycling, energy flow within the food web, biodiversity, carbon sequestration, and MAF stability. This comprehensive review describes trophic interactions at all levels of ecological organisation in tropical, temperate, and cold‐water MAFs. It examines the strengths and weaknesses of available tools for estimating the heterotrophic capacities of the foundational species in MAFs. It then discusses the threats that climate change poses to heterotrophic processes. Finally, it presents strategies for improving trophic interactions and heterotrophy, which can help to maintain the health and resilience of MAFs.

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Symbiodiniaceae Are the First Site of Heterotrophic Nitrogen Assimilation in Reef-Building Corals

Abstract: Coral reefs rely upon the highly optimized nutritional symbiosis between corals and Symbiodiniaceae dinoflagellates. Heterotrophic feeding on plankton is key to the resistance of corals to environmental stress.

Cited by 12 publications

References 55 publications

Tracing the fate of seabird‐derived nitrogen in a coral reef using nitrate and coral skeleton nitrogen isotopes

Tracing the fate of seabird‐derived nitrogen in a coral reef using nitrate and coral skeleton nitrogen isotopes

Irradiance driven trophic plasticity in the coral Madracis pharensis from the Eastern Mediterranean

Heterotrophy in marine animal forests in an era of climate change

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