Diazotrophs: a non-negligible source of nitrogen for the tropical coral <i>Stylophora pistillata</i>

Benavides, Mar; Houlbrèque, Fanny; Camps, Mercedes; Lorrain, Anne; Grosso, Olivier; Bonnet, Sophie

doi:10.1242/jeb.139451

Cited by 46 publications

(95 citation statements)

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“…However, it has been demonstrated that zooxanthellae account for most of the NH + 4 uptake with assimilation rates 14-23 times faster compared to the coral host (Pernice et al, 2012). This is in agreement with previous N 2 fixation studies on tropical corals demonstrating that DDN is primarily used by the zooxanthellae (Lesser et al, 2007;Benavides et al, 2016). Lesser et al (2007) observed a significantly depleted natural δ 15 N signature in the zooxanthellae, but not in the animal tissue, when the corals were associated with diazotrophs.…”

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

confidence: 88%

“…So far only few studies have provided evidence of the assimilation of DDN by corals either using the natural δ 15 N signature of corals or the 15 N 2 labeling technique (Lesser et al, 2007;Grover et al, 2014;Benavides et al, 2016;Bednarz et al, 2017). Grover et al (2014) did not detect DDN assimilation by the coral, while the other studies did, underlining that DDN assimilation by corals is not a straightforward process but can be very variable depending on the current environmental conditions and the associated diazotrophic community.…”

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

confidence: 96%

“…This miscalculation has been shown to result in a severe underestimation of pelagic N 2 fixation rates (Großkopf et al, 2012), and can be also a problem when estimating coral-associated N 2 fixation (Grover et al, 2014;Benavides et al, 2016). To avoid this, Mohr et al (2010) proposed pre-dissolving 15 N 2 into seawater and hence adding the tracer in its liquid form to samples prior to their incubation, with the aim of maintaining the 15 N enrichment of the source N 2 pool constant overtime.…”

Section: N 2 Fixation In Coral Reef Ecosystems Description Of N 2 Fixmentioning

confidence: 99%

“…A depleted δ 15 N signature indicates that at least part of assimilated nitrogen is derived from DDN. 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).…”

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

confidence: 99%

“…Benavides et al (2016) demonstrated that corals assimilate DDN via active feeding on planktonic free-living diazotrophs. Corals are passive suspension feeders and trap particles and bacteria in their mucus as a nutrient source (Wild et al, 2004).…”

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

confidence: 99%

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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: 88%

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

confidence: 96%

Section: N 2 Fixation In Coral Reef Ecosystems Description Of N 2 Fixmentioning

confidence: 99%

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

confidence: 99%

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

confidence: 99%

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

2017

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Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa

Rädecker

Pogoreutz

Ziegler

et al. 2017

Ecology and Evolution

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The productivity of coral reefs in oligotrophic tropical waters is sustained by an efficient uptake and recycling of nutrients. In reef‐building corals, the engineers of these ecosystems, this nutrient recycling is facilitated by a constant exchange of nutrients between the animal host and endosymbiotic photosynthetic dinoflagellates (zooxanthellae), bacteria, and other microbes. Due to the complex interactions in this so‐called coral holobiont, it has proven difficult to understand the environmental limitations of productivity in corals. Among others, the micronutrient iron has been proposed to limit primary productivity due to its essential role in photosynthesis and bacterial processes. Here, we tested the effect of iron enrichment on the physiology of the coral Pocillopora verrucosa from the central Red Sea during a 12‐day experiment. Contrary to previous reports, we did not see an increase in zooxanthellae population density or gross photosynthesis. Conversely, respiration rates were significantly increased, and microbial nitrogen fixation was significantly decreased. Taken together, our data suggest that iron is not a limiting factor of primary productivity in Red Sea corals. Rather, increased metabolic demands in response to iron enrichment, as evidenced by increased respiration rates, may reduce carbon (i.e., energy) availability in the coral holobiont, resulting in reduced microbial nitrogen fixation. This decrease in nitrogen supply in turn may exacerbate the limitation of other nutrients, creating a negative feedback loop. Thereby, our results highlight that the effects of iron enrichment appear to be strongly dependent on local environmental conditions and ultimately may depend on the availability of other nutrients.

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Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses

Ferrier‐Pagés

Leal

2018

Ecology and Evolution

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Mutualistic nutritional symbioses are widespread in marine ecosystems. They involve the association of a host organism (algae, protists, or marine invertebrates) with symbiotic microorganisms, such as bacteria, cyanobacteria, or dinoflagellates. Nutritional interactions between the partners are difficult to identify in symbioses because they only occur in intact associations. Stable isotope analysis (SIA) has proven to be a useful tool to highlight original nutrient sources and to trace nutrients acquired by and exchanged between the different partners of the association. However, although SIA has been extensively applied to study different marine symbiotic associations, there is no review taking into account of the different types of symbiotic associations, how they have been studied via SIA, methodological issues common among symbiotic associations, and solutions that can be transferred from one type of association with another. The present review aims to fill such gaps in the scientific literature by summarizing the current knowledge of how isotopes have been applied to key marine symbioses to unravel nutrient exchanges between partners, and by describing the difficulties in interpreting the isotopic signal. This review also focuses on the use of compound‐specific stable isotope analysis and on statistical advances to analyze stable isotope data. It also highlights the knowledge gaps that would benefit from future research.

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

Cited by 46 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?

Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa

Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses

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