A Short Comparison of Two Marine Planktonic Diazotrophic Symbioses Highlights an Un-quantified Disparity

Caputo, Andrea; Stenegren, Marcus; Pernice, Massimo C.; Foster, Rachel A.

doi:10.3389/fmars.2018.00002

Cited by 18 publications

(15 citation statements)

References 53 publications

(98 reference statements)

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“…However, it now appears that some diazotrophic groups may be more sensitive to this effect than others, thereby influencing the composition of diazotroph assemblages in waters bearing significant NO x concentrations or subject to NO x inputs Moisander et al, 2012;Mulholland et al, 2001;Voss et al, 2006). For example, certain symbiotic diazotrophs appear to lack genes necessary to transport and assimilate some forms of dissolved inorganic N (Caputo et al, 2018) and may thus be less responsive to changes in ambient N concentrations than other diazotrophs. Both temperature and NO x concentrations …”

Section: Resultsmentioning

confidence: 99%

High Rates of N₂ Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

Mulholland

Bernhardt

Widner

et al. 2019

Global Biogeochemical Cycles

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Dinitrogen (N2) fixation can alleviate N limitation of primary productivity by introducing fixed nitrogen (N) to the world's oceans. Although measurements of pelagic marine N2 fixation are predominantly from oligotrophic oceanic regions, where N limitation is thought to favor growth of diazotrophic microbes, here we report high rates of N2 fixation from seven cruises spanning four seasons in temperate, western North Atlantic coastal waters along the North American continental shelf between Cape Hatteras and Nova Scotia, an area representing 6.4% of the North Atlantic continental shelf area. Integrating average areal rates of N2 fixation during each season and for each domain in the study area, the estimated N input from N2 fixation to this temperate shelf system is 0.02 Tmol N/year, an amount equivalent to that previously estimated for the entire North Atlantic continental shelf. Unicellular group A cyanobacteria (UCYN‐A) were most often the dominant diazotrophic group expressing nifH, a gene encoding the nitrogenase enzyme, throughout the study area during all seasons. This expands the domain of these diazotrophs to include coastal waters where dissolved N concentrations are not always depleted. Further, the high rates of N2 fixation and diazotroph diversity along the western North Atlantic continental shelf underscore the need to reexamine the biogeography and the activity of diazotrophs along continental margins. Accounting for this substantial but previously overlooked source of new N to marine systems necessitates revisions to global marine N budgets.

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Section: Resultsmentioning

confidence: 99%

High Rates of N₂ Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

Mulholland

Bernhardt

Widner

et al. 2019

Global Biogeochemical Cycles

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“…The remaining cells in the trichome, called vegetative cells, are phototrophic and divide, whereas heterocysts do not. Despite the seemingly ideal combination of cells specialized for carbon (C) and nitrogen (N) acquisition, the trichomes have rarely been observed as free-living organisms in the marine environment [20,21]. This indicates that the trichomes receive some essential nutrients, which allow them to grow more efficiently as a part of the symbiosis.…”

Section: Introductionmentioning

confidence: 99%

Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N2 Fixation by Symbiotic Heterocystous Cyanobacteria

Inomura

Follett

Masuda

et al. 2020

Plants

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Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N2) fixation. It is inferred that the growth of the trichomes is also supported by the host, but the support mechanism has not been fully quantified. Here, we develop a coarse-grained, cellular model of the symbiosis between Hemiaulus and Richelia (one of the major DDAs), which shows that carbon (C) transfer from the diatom enables a faster growth and N2 fixation rate by the trichomes. The model predicts that the rate of N2 fixation is 5.5 times that of the hypothetical case without nitrogen (N) transfer to the host diatom. The model estimates that 25% of fixed C from the host diatom is transferred to the symbiotic trichomes to support the high rate of N2 fixation. In turn, 82% of N fixed by the trichomes ends up in the host. Modeled C fixation from the vegetative cells in the trichomes supports only one-third of their total C needs. Even if we ignore the C cost for N2 fixation and for N transfer to the host, the total C cost of the trichomes is higher than the C supply by their own photosynthesis. Having more trichomes in a single host diatom decreases the demand for N2 fixation per trichome and thus decreases their cost of C. However, even with five trichomes, which is about the highest observed for Hemiaulus and Richelia symbiosis, the model still predicts a significant C transfer from the diatom host. These results help quantitatively explain the observed high rates of growth and N2 fixation in symbiotic trichomes relative to other aquatic diazotrophs.

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“…There are a variety of reasons organisms may fix N 2 despite its energetic costs. Certain organisms, including some eukaryote symbionts, lack the genetic ability to reduce nitrate (NO 3 − ; Caputo et al, 2018); investing in NO 3 − assimilation machinery may be unfavorable for diazotrophs already growing on N 2 (Karl et al, 2002), and some diazotrophs may use N 2 fixation as a mechanism for regulating intracellular state (Bombar et al, 2016), potentially decoupling its activity from N demand satiety. One energetic complication is that nitrogenase, the enzyme that mediates N 2 fixation, is permanently inhibited by O 2 (Postgate, 1998), and oxygenic diazotrophs as well as those inhabiting oxic environments must invest in O 2 avoidance strategies to minimize nitrogenase turnover (Vitousek et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Dinitrogen Fixation Across Physico‐Chemical Gradients of the Eastern Tropical North Pacific Oxygen Deficient Zone

Selden

Mulholland

Bernhardt

et al. 2019

Global Biogeochemical Cycles

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The Eastern Tropical North Pacific Ocean hosts one of the world's largest oceanic oxygen deficient zones (ODZs). Hot spots for reactive nitrogen (Nr) removal processes, ODZs generate conditions proposed to promote Nr inputs via dinitrogen (N2) fixation. In this study, we quantified N2 fixation rates by 15N tracer bioassay across oxygen, nutrient, and light gradients within and adjacent to the ODZ. Within subeuphotic oxygen‐deplete waters, N2 fixation was largely undetectable; however, addition of dissolved organic carbon stimulated N2 fixation in suboxic (<20 μmol/kg O2) waters, suggesting that diazotroph communities are likely energy limited or carbon limited and able to fix N2 despite high ambient concentrations of dissolved inorganic nitrogen. Elevated rates (>9 nmol N·L−1·day−1) were also observed in suboxic waters near volcanic islands where N2 fixation was quantifiable to 3,000 m. Within the overlying euphotic waters, N2 fixation rates were highest near the continent, exceeding 500 μmol N·m−2·day−1 at one third of inshore stations. These findings support the expansion of the known range of diazotrophs to deep, cold, and dissolved inorganic nitrogen‐replete waters. Additionally, this work bolsters calls for the reconsideration of ocean margins as important sources of Nr. Despite high rates at some inshore stations, regional N2 fixation appears insufficient to compensate for Nr loss locally as observed previously in the Eastern Tropical South Pacific ODZ.

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A Short Comparison of Two Marine Planktonic Diazotrophic Symbioses Highlights an Un-quantified Disparity

Cited by 18 publications

References 53 publications

High Rates of N₂ Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

High Rates of N₂ Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N2 Fixation by Symbiotic Heterocystous Cyanobacteria

Dinitrogen Fixation Across Physico‐Chemical Gradients of the Eastern Tropical North Pacific Oxygen Deficient Zone

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A Short Comparison of Two Marine Planktonic Diazotrophic Symbioses Highlights an Un-quantified Disparity

Cited by 18 publications

References 53 publications

High Rates of N2 Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

High Rates of N2 Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N2 Fixation by Symbiotic Heterocystous Cyanobacteria

Dinitrogen Fixation Across Physico‐Chemical Gradients of the Eastern Tropical North Pacific Oxygen Deficient Zone

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High Rates of N₂ Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy

High Rates of N₂ Fixation in Temperate, Western North Atlantic Coastal Waters Expand the Realm of Marine Diazotrophy