Marine Non-Cyanobacterial Diazotrophs: Moving beyond Molecular Detection

Bombar, Deniz; Paerl, Ryan W.; Riemann, Lasse

doi:10.1016/j.tim.2016.07.002

Cited by 146 publications

(182 citation statements)

References 105 publications

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“…The fact that rhizobia sequences could be only retrieved from the coral tissue could indicate a compartmental distribution of diazotrophs within the coral holobiont. For example, legumeassociated rhizobia only fix N 2 in oxygen-depleted conditions, thus it is plausible that coral-associated rhizobia only succeed at fixing N 2 when the tissues experience microaerophilic conditions at night (but non-cyanobacterial diazotrophs may fix N 2 actively at a wide range of oxygen concentrations; Bombar et al, 2016). Nevertheless, high concentrations have also been found in the mucus layer of Acropora sp.…”

Section: Diversity Of Diazotrophs In Tropical Coralsmentioning

confidence: 99%

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: Diversity Of Diazotrophs In Tropical Coralsmentioning

confidence: 99%

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

2017

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“…This has inspired many investigators to hypothesize that global N inputs by BNF could potentially be much higher than previously thought. However, the ecology and actual contribution of heterotrophic diazotrophs to oceanic BNF is still largely elusive (Bombar et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Filtration via Conventional Glass Fiber Filters in 15N2 Tracer Assays Fails to Capture All Nitrogen-Fixing Prokaryotes

et al. 2018

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Biological dinitrogen fixation (BNF) represents a major input of reduced nitrogen (N) to the oceans. Accurate direct measurements of BNF rates are crucial for reliably determining the biogeochemical significance of diazotrophy at local and global scales. Traditionally, borosilicate glass fiber filters (GF/F, Whatman) with a nominal pore size of 0.7 µm are used to collect suspended particles by filtration after incubations with added 15 N 2 tracer. We carried out BNF experiments in the Baltic Sea, Danish coastal waters, and the Pacific Ocean comparing the retentive characteristics of precombusted GF/F filters with newer Advantec glass fiber filters which have a smaller nominal pore size of 0.3 µm. Where BNF was detected, rates were nearly always higher, and sometimes even exclusively detectable, when using Advantec filters. In the majority of samples across tested habitats, significantly more cells were lost to GF/F filtrate (average = 51%, range = 10-70% of cells) than to Advantec filtrate (average = 40%, range = 10-54%). Using Illumina sequencing of nitrogenase (nifH) gene amplicons, we show that diazotroph communities can markedly differ between bulk water and filtrates from GF/F and Advantec filtrations, suggesting that different diazotrophs can pass through the filter types. In order to reduce the potential underestimations of BNF due to filtration loss of diazotrophs, we recommend using Advantec filters or alternatively silver membranes with 0.2 µm pore size, especially in waters expected to be inhabited by relatively small, unicellular diazotrophs.

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“…Aphotic N 2 fixation may contribute significantly to global fixed nitrogen inputs if widespread throughout the ocean's mesopelagic zone (or deeper). Unfortunately, our ability to assess this contribution remains hindered by the lack of specific N 2 fixation methods and our poor understanding of the ecophysiology of noncyanobacterial diazotrophs (Bombar et al, 2016;Moisander et al, 2017). 30 N 2 fixation rates in aphotic environments correlate with different DOM compound groups in different regions (Benavides et al, 2015;, and nifH gene expression varies among noncyanobacterial diazotroph phylotypes when exposed to conditions presumed to enhance their N 2 fixation activity .…”

Section: Discussionmentioning

confidence: 99%

“…25 Non-cyanobacterial diazotrophs span the four established nifH gene clusters (Chien and Zinder, 1996), are the most numerous in nifH gene databases (Farnelid and Riemann, 2008), and are spread throughout the global ocean Farnelid et al, 2011;Langlois et al, 2015;Messer et al, 2015). As discussed in Bombar et al (2016), the growth and activity of non-cyanobacterial diazotrophs may be controlled by (i) the presence of oxygen -because oxygen destroys the nitrogenase 30 enzyme, (ii) the availability of fixed nitrogen because N 2 fixation becomes too energetically expensive when reduced nitrogen forms are readily available in the environment, and (iii) the availability of energy because non-cyanobacterial diazotrophs may not be able to photosynthesize and thus rely on external fixed carbon sources. However, aphotic diazotrophic activity has been found both in oxygen deficient regions such as the oxygen minimum zone of the Eastern Tropical South Pacific (Bonnet et al,35 2013; Loescher et al, 2014), and fully oxygenated mesopelagic waters in the Mediterranean Sea Biogeosciences Discuss., https://doi.org /10.5194/bg-2017-542 Manuscript under review for journal Biogeosciences Discussion started: 5 January 2018 c Author(s) 2018.…”

mentioning

confidence: 99%

Aphotic N<sub>2</sub> fixation along an oligotrophic to ultraoligotrophic transect in the Western Tropical South Pacific Ocean

Benavides¹,

Shoemaker²,

Moisander³

et al. 2018

Preprint

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Abstract.The western tropical South Pacific (WTSP) Ocean has been recognized as a global hotspot of dinitrogen 25 (N 2 ) fixation. Here, as in other marine environments across the oceans, N 2 fixation studies have focused in the sunlit layer. However, studies have confirmed the importance of aphotic N 2 fixation activity, although until now only one had been performed in the WTSP. In order to increase our knowledge of aphotic N 2 fixation in the WTSP, here we measure N 2 fixation rates and identify diazotrophic phylotypes in the mesopelagic layer along a transect spanning from New Caledonia to French that the distribution of aphotic diazotroph communities is to some extent controlled by water mass structure. While the data available is still too scarce to elucidate the distribution and controls of 5 mesopelagic non-cyanobacterial diazotrophs in the WTSP, their prevalence in the mesopelagic layer and the consistent detection of active N 2 fixation activity at all depths sampled during our study suggest that aphotic N 2 fixation may contribute significantly to fixed nitrogen inputs in this area.

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Marine Non-Cyanobacterial Diazotrophs: Moving beyond Molecular Detection

Cited by 146 publications

References 105 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?

Filtration via Conventional Glass Fiber Filters in 15N2 Tracer Assays Fails to Capture All Nitrogen-Fixing Prokaryotes

Aphotic N<sub>2</sub> fixation along an oligotrophic to ultraoligotrophic transect in the Western Tropical South Pacific Ocean

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Marine Non-Cyanobacterial Diazotrophs: Moving beyond Molecular Detection

Cited by 146 publications

References 105 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?

Filtration via Conventional Glass Fiber Filters in 15N2 Tracer Assays Fails to Capture All Nitrogen-Fixing Prokaryotes

Aphotic N&lt;sub&gt;2&lt;/sub&gt; fixation along an oligotrophic to ultraoligotrophic transect in the Western Tropical South Pacific Ocean

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Aphotic N<sub>2</sub> fixation along an oligotrophic to ultraoligotrophic transect in the Western Tropical South Pacific Ocean