Highly Dynamic Cellular-Level Response of Symbiotic Coral to a Sudden Increase in Environmental Nitrogen

Kopp, Christophe; Pernice, Mathieu; Domart‐Coulon, Isabelle; Djédiat, Chakib; Spangenberg, Jorge E.; Alexander, Duncan T. L.; Hignette, M.; Méziane, Tarik; Meibom, Anders

doi:10.1128/mbio.00052-13

Cited by 141 publications

(173 citation statements)

References 50 publications

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“…Benavides et al (2016) used 15 N 2 labeling and detected after a 4 h incubation period DDN assimilation only in the zooxanthellae and not in the animal tissue. Once DDN is assimilated by the zooxanthellae it enters the internal nitrogen recycling loop of the coral holobiont and will be translocated as recycled organic nitrogen from the zooxanthellae to the coral host (Kopp et al, 2013). This suggests that likely more than 4 h incubation time are needed in order to detect DDN assimilation by the host and is consistent with an observed time lag of 6 h for delayed nitrogen translocation from the zooxanthellae to the host (Kopp et al, 2013).…”

Section: Mechanisms Of Ddn Uptake and Transfer Among Compartments Of supporting

confidence: 59%

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

2017

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Coral reefs are highly productive ecosystems thriving in nutrient-poor waters. Their productivity depends largely on the availability of nitrogen, the proximate limiting nutrient for primary production. In reefs, the major nitrogen pathways include regeneration, nitrification, ammonification and dinitrogen (N 2 ) fixation. N 2 fixation is performed by prokaryotes called "diazotrophs" that abound in coral rubbles, sandy bottoms, microbial mats, or seagrass meadows. Corals, which are the main reef builders, have developed a partnership with dinoflagellates which transform dissolved inorganic nitrogen into amino acids and protein, and with diazotrophs to gain diazotrophically-derived nitrogen (DDN). Pioneering studies found active diazotrophic cyanobacteria in the corals' mucus and/or tissue, and later high throughput sequencing efforts have described diverse communities of non-cyanobacterial diazotrophs associated with scleractinian corals. Yet, the metabolic processes behind these associations and how they benefit corals are currently not well understood. While genomic studies describe the diversity of diazotrophs and isotopic tracer experiments quantify N 2 fixation rates, combined advanced methods are needed to elucidate the mechanisms behind the transfer of DDN to the coral holobiont and whether these mechanisms change according to the identity of the diazotrophs or coral species. Here we review our current knowledge on N 2 fixation in corals: the diversity and localization of diazotrophs in the coral holobiont, the environmental factors controlling N 2 fixation, the fate of DDN within the coral symbiosis as well as its potential role in coral resilience. We finally summarize the unknowns: are the diversity, abundance and localization of diazotrophs within the holobiont species-and/or site-specific? Do they have an impact on DDN production? What are the metabolic mechanisms implicated? Do they change spatially, temporally or according to environmental factors? We encourage scientists to undertake research efforts to tackle these questions in order to shed light on nitrogen cycling in reef ecosystems and to understand if coral-associated N 2 fixation can improve coral's resilience in the face of climate change.

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Section: Mechanisms Of Ddn Uptake and Transfer Among Compartments Of supporting

confidence: 59%

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

2017

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“…Zooxanthellae have the ability to take up and retain nitrogen from surrounding water (Grover and Maguer, 2002;Rädecker et al, 2015) and transfer it to the host (Kopp et al, 2013); corals can also obtain nitrogen via the ingestion of external food sources (Houlbreque and Ferrier-Pages, 2009); hence, it was important to calculate the assimilation of nitrogen by the tissue and the zooxanthellae separately. Nitrogen assimilation rates were calculated as described in Montoya et al (1996) (i) in experiment 1 the source pool is seawater and the isotopic enrichment of the filtered seawater added to the containers, (ii) in experiment 2, it is the Cyanothece culture and (iii) in experiment 3 it is the natural planktonic assemblage.…”

Section: N Assimilationmentioning

confidence: 99%

Diazotrophs: a non-negligible source of nitrogen for the tropical coral Stylophora pistillata

Benavides

Houlbrèque²,

Camps

et al. 2016

Journal of Experimental Biology

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Corals are mixotrophs: they are able to fix inorganic carbon through the activity of their symbiotic dinoflagellates and to gain nitrogen from predation on plankton and uptake of dissolved organic and inorganic nutrients. They also live in close association with diverse diazotrophic communities, inhabiting their skeleton, tissue and mucus layer, which are able to fix dinitrogen (N 2 ). The quantity of fixed N 2 transferred to the corals and its distribution within coral compartments as well as the quantity of nitrogen assimilated through the ingestion of planktonic diazotrophs are still unknown. Here, we quantified nitrogen assimilation via (i) N 2 fixation by symbiont diazotrophs, (ii) ingestion of cultured unicellular diazotrophs and (iii) ingestion of natural planktonic diazotrophs. We estimate that the ingestion of diazotrophs provides 0.76±0.15 µg N cm, suggesting that diazotrophs represent a non-negligible source of nitrogen for scleractinian corals.

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“…On the other hand, Symbiodinium spp. is efficient in the uptake of fixed N (Kopp et al 2013), and cell division rates are faster in corals that show high N 2 fixation activity (Lesser et al 2007). Hence, N 2 fixation may play a key role in regulating the coral−dinoflagellate symbiosis.…”

Section: Introductionmentioning

confidence: 99%

Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix

Rädecker¹,

Meyer²,

Bednarz³

et al. 2014

Mar. Ecol. Prog. Ser.

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Since productivity and growth of coral-associated dinoflagellate algae is nitrogen (N)-limited, dinitrogen (N 2 ) fixation by coral-associated microbes is likely crucial for maintaining the coral−dinoflagellate symbiosis. It is thus essential to understand the effects future climate change will have on N 2 fixation by the coral holobiont. This laboratory study is the first to investigate short-term effects of ocean acidification on N 2 fixation activity associated with the tropical, hermatypic coral Seriatopora hystrix using the acetylene reduction assay in combination with calcification measurements. Findings reveal that simulated ocean acidification ( pCO 2 1080 µatm) caused a rapid and significant decrease (53%) in N 2 fixation rates associated with S. hystrix compared to the present day scenario ( pCO 2 486 µatm). In addition, N 2 fixation associated with the coral holobiont showed a positive exponential relationship with its calcification rates. This suggests that even small declines in calcification rates of hermatypic corals under high CO 2 conditions may result in decreased N 2 fixation activity, since these 2 processes may compete for energy in the coral holobiont. Ultimately, an intensified N limitation in combination with a decline in skeletal growth may trigger a negative feedback loop on coral productivity exacerbating the negative long-term effects of ocean acidification.

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Highly Dynamic Cellular-Level Response of Symbiotic Coral to a Sudden Increase in Environmental Nitrogen

Cited by 141 publications

References 50 publications

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

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

Diazotrophs: a non-negligible source of nitrogen for the tropical coral Stylophora pistillata

Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix

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