Dissolved organic matter stimulates N2 fixation and <i>nifH</i> gene expression in <i>Trichodesmium</i>

Benavides, Mar; Duhamel, Solange; Wambeke, F. Van; Shoemaker, Katyanne M.; Moisander, Pia H.; Salamon, Ellen R.; Riemann, Lasse

doi:10.1093/femsle/fnaa034

Cited by 20 publications

(17 citation statements)

References 65 publications

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“…4 b,c). Trichodesmium could have responded positively to DOP inputs as observed elsewhere 31 , 32 , but in our study DOP concentrations of clear and sewage waters were not significantly different (Table 1 ). We cannot exclude however, the possibility that there were toxic components in sewage waters that may have locally promoted the death of Trichodesmium close to the coast, as wastewaters are known to impair the metabolic activity of phytoplankton 33 .…”

Section: Resultssupporting

confidence: 63%

Untreated sewage outfalls do not promote Trichodesmium blooms in the coasts of the Canary Islands

Benavides

Arı́stegui

2020

Sci Rep

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During the summer of 2017, recurrent extensive blooms of the diazotrophic cyanobacterium Trichodesmium invaded the beaches and coastal waters of the Canary Islands, causing great social alarm. Some local media and public sectors ascribed, without any strong scientific evidence, the origin and reactivation of these blooms to untreated sewage outfalls distributed along the coasts. In order to test whether sewage outfalls could have any influence on the metabolic activity of Trichodesmium, we performed 13C and 15N2 uptake experiments with colonies experiencing three different bloom development stages, incubated both with clear seawater and sewage water from an outfall south of Gran Canaria island. Our results showed that sewage outfalls did not promote any increase in dinitrogen (N2) fixation in Trichodesmium, supporting the hypothesis that decaying blooms were generated offshore and transported shoreward by local currents and winds, accumulating mostly leeward of the islands. The combination of unusually warm seawater temperatures, enhanced and sustained stratification of the upper water column and recurrent dust deposition events would have favored the development of the Trichodesmium blooms, which lasted for at least four months.

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Section: Resultssupporting

confidence: 63%

Untreated sewage outfalls do not promote Trichodesmium blooms in the coasts of the Canary Islands

Benavides

Arı́stegui

2020

Sci Rep

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“…We cannot rule out that some of the colonizing phototrophic (cyanobacteria) diazotrophs were mixotrophs, namely bacteria that can “switch” between heterotrophic metabolism to carbon fixation via photosynthesis, rather than obligatory phototrophs. Recent studies demonstrated that the cyanobacterium Trichodesmium , previously characterized as phototrophs, may, in fact, use mixotrophic metabolism ( Benavides et al, 2017 , 2020 ). Similarly, the unicellular cyanobacterial diazotroph Cyanothece have been shown to take up carbohydrates and amino acids ( Feng et al, 2010 ).…”

Section: Resultsmentioning

confidence: 99%

Heterotrophic Nitrogen Fixation at the Hyper-Eutrophic Qishon River and Estuary System

et al. 2020

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Planktonic heterotrophic diazotrophs (N 2-fixers) are widely distributed in marine and freshwater systems, yet limited information is available on their activity, especially in environments with adverse conditions for diazotrophy (e.g., N-rich and oxygenated). Here, we followed the localization and activity of heterotrophic diazotrophs in the hyper-eutrophic N-rich Qishon River-an environment previously considered to be unfavorable for diazotrophy. Our results indicate high heterotrophic N 2 fixation rates (up to 6.9 nmol N L −1 d −1), which were approximately three fold higher at an upstream location (freshwater) compared to an estuary (brackish) site. Further, active heterotrophic diazotrophs were capture associated with free-floating aggregates by a newly developed immunolocalization approach. These findings provide new insights on the activity of heterotrophic diazotrophs on aggregates in environments previously considered with adverse conditions for diazotrophy. Moreover, these new insights may be applicable to other aquatic regimes worldwide with similar N-rich/oxygenated conditions that should potentially inhibit N 2 fixation.

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“…2h ). Phytoplankton and bacterioplankton are known to release dissolved substances, such as dissolved organic N, P, and C [ 59 ], B vitamins [ 60 ], and compounds that scavenge dissolved iron (e.g., siderophores, [ 61 ]), which have the potential to stimulate the fixation of CO 2 or N 2 by haptophytes and diazotrophs, respectively, even on these short time scales (<48 h; [ 62 – 64 ]). Vitamin B 12 is of particular interest, given that haptophytes are suspected to be B 12 auxotrophs [ 65 ].…”

Section: Discussionmentioning

confidence: 99%

Unusual marine cyanobacteria/haptophyte symbiosis relies on N2 fixation even in N-rich environments

et al. 2020

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The microbial fixation of N2 is the largest source of biologically available nitrogen (N) to the oceans. However, it is the most energetically expensive N-acquisition process and is believed inhibited when less energetically expensive forms, like dissolved inorganic N (DIN), are available. Curiously, the cosmopolitan N2-fixing UCYN-A/haptophyte symbiosis grows in DIN-replete waters, but the sensitivity of their N2 fixation to DIN is unknown. We used stable isotope incubations, catalyzed reporter deposition fluorescence in-situ hybridization (CARD-FISH), and nanoscale secondary ion mass spectrometry (nanoSIMS), to investigate the N source used by the haptophyte host and sensitivity of UCYN-A N2 fixation in DIN-replete waters. We demonstrate that under our experimental conditions, the haptophyte hosts of two UCYN-A sublineages do not assimilate nitrate (NO3−) and meet little of their N demands via ammonium (NH4+) uptake. Instead the UCYN-A/haptophyte symbiosis relies on UCYN-A N2 fixation to supply large portions of the haptophyte’s N requirements, even under DIN-replete conditions. Furthermore, UCYN-A N2 fixation rates, and haptophyte host carbon fixation rates, were at times stimulated by NO3− additions in N-limited waters suggesting a link between the activities of the bulk phytoplankton assemblage and the UCYN-A/haptophyte symbiosis. The results suggest N2 fixation may be an evolutionarily viable strategy for diazotroph–eukaryote symbioses, even in N-rich coastal or high latitude waters.

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Dissolved organic matter stimulates N2 fixation and nifH gene expression in Trichodesmium

Cited by 20 publications

References 65 publications

Untreated sewage outfalls do not promote Trichodesmium blooms in the coasts of the Canary Islands

Untreated sewage outfalls do not promote Trichodesmium blooms in the coasts of the Canary Islands

Heterotrophic Nitrogen Fixation at the Hyper-Eutrophic Qishon River and Estuary System

Unusual marine cyanobacteria/haptophyte symbiosis relies on N2 fixation even in N-rich environments

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