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Light-limited growth rate modulates nitrate inhibition of dinitrogen fixation in the marine unicellular cyanobacterium Crocosphaera watsonii.

Garcia NS, Hutchins DA - PLoS ONE (2014)

Bottom Line: In high-light-acclimated, fast-growing cultures, NO3- did not inhibit N2-fixation rates in comparison with cultures growing on N2 alone.Instead NO3- supported even faster growth, indicating that the cellular assimilation rate of N2 alone (i.e. dinitrogen reduction) could not support the light-specific maximum growth rate of Crocosphaera.When growth was severely light-limited, NO3- did not support faster growth rates but instead inhibited N2-fixation rates by 55% relative to controls.

View Article: PubMed Central - PubMed

Affiliation: Marine and Environmental Biology, Department of Biological Sciences, University of Southern California, Los Angeles, CA, United States of America.

ABSTRACT
Biological N2 fixation is the dominant supply of new nitrogen (N) to the oceans, but is often inhibited in the presence of fixed N sources such as nitrate (NO3-). Anthropogenic fixed N inputs to the ocean are increasing, but their effect on marine N2 fixation is uncertain. Thus, global estimates of new oceanic N depend on a fundamental understanding of factors that modulate N source preferences by N2-fixing cyanobacteria. We examined the unicellular diazotroph Crocosphaera watsonii (strain WH0003) to determine how the light-limited growth rate influences the inhibitory effects of fixed N on N2 fixation. When growth (µ) was limited by low light (µ = 0.23 d-1), short-term experiments indicated that 0.4 µM NH4+ reduced N2-fixation by ∼90% relative to controls without added NH4+. In fast-growing, high-light-acclimated cultures (µ = 0.68 d-1), 2.0 µM NH4+ was needed to achieve the same effect. In long-term exposures to NO3-, inhibition of N2 fixation also varied with growth rate. In high-light-acclimated, fast-growing cultures, NO3- did not inhibit N2-fixation rates in comparison with cultures growing on N2 alone. Instead NO3- supported even faster growth, indicating that the cellular assimilation rate of N2 alone (i.e. dinitrogen reduction) could not support the light-specific maximum growth rate of Crocosphaera. When growth was severely light-limited, NO3- did not support faster growth rates but instead inhibited N2-fixation rates by 55% relative to controls. These data rest on the basic tenet that light energy is the driver of photoautotrophic growth while various nutrient substrates serve as supports. Our findings provide a novel conceptual framework to examine interactions between N source preferences and predict degrees of inhibition of N2 fixation by fixed N sources based on the growth rate as controlled by light.

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Changes in nitrate (triangles) and cell concentrations (circles) in cultures of Crocosphaera watsonii (WH0003) in long-term exposure experiments.Cultures were grown in steady state under (a) high light (175 µmol quanta m−2 s−1) and (b) low light (25 µmol quanta m−2 s−1) with added nitrate (30 µmol L−1; open symbols) or with N2 only (closed symbols). *Calculated NO3− concentrations (see Methods section for details). Error bars represent standard deviations on means from 3 culture replicates.
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pone-0114465-g003: Changes in nitrate (triangles) and cell concentrations (circles) in cultures of Crocosphaera watsonii (WH0003) in long-term exposure experiments.Cultures were grown in steady state under (a) high light (175 µmol quanta m−2 s−1) and (b) low light (25 µmol quanta m−2 s−1) with added nitrate (30 µmol L−1; open symbols) or with N2 only (closed symbols). *Calculated NO3− concentrations (see Methods section for details). Error bars represent standard deviations on means from 3 culture replicates.

Mentions: In high-light-acclimated cultures, long-term exposure to 30 µM NO3− yielded significantly higher growth rates (µ = 0.87 d−1) than those in control cultures without added NO3− (µ = 0.68 d−1; p<0.05), indicating that growth was limited by the N2-assimilation rate (Fig. 2a). Diminishing NO3− concentrations over time suggested that NO3−-assimilation rates in fast-growing cultures (µ = 0.87 d−1) were 2.8 times higher than those in slow-growing cultures (µ = 0.23 d−1; Fig. 3a; p<0.05), but the contribution of NO3− to the total daily N assimilation still varied as a function of growth rate. In high-light-acclimated cultures exposed to NO3− (µ = 0.87 d−1), NO3− assimilation represented 40% of the total daily N assimilation while N2 assimilation represented 60% (Fig. 2b). When combined, NO3− and N2 assimilation yielded a higher total daily N-assimilation rate (187 fmol N cell−1 d−1) than that in the control treatment growing on N2 only (122 fmol N cell−1 d−1; p<0.05; Fig. 2b). Furthermore, N2-fixation rates in cultures with added NO3− were not significantly different than those in control cultures without NO3− (p<0.05; Fig. 2b).


Light-limited growth rate modulates nitrate inhibition of dinitrogen fixation in the marine unicellular cyanobacterium Crocosphaera watsonii.

Garcia NS, Hutchins DA - PLoS ONE (2014)

Changes in nitrate (triangles) and cell concentrations (circles) in cultures of Crocosphaera watsonii (WH0003) in long-term exposure experiments.Cultures were grown in steady state under (a) high light (175 µmol quanta m−2 s−1) and (b) low light (25 µmol quanta m−2 s−1) with added nitrate (30 µmol L−1; open symbols) or with N2 only (closed symbols). *Calculated NO3− concentrations (see Methods section for details). Error bars represent standard deviations on means from 3 culture replicates.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263673&req=5

pone-0114465-g003: Changes in nitrate (triangles) and cell concentrations (circles) in cultures of Crocosphaera watsonii (WH0003) in long-term exposure experiments.Cultures were grown in steady state under (a) high light (175 µmol quanta m−2 s−1) and (b) low light (25 µmol quanta m−2 s−1) with added nitrate (30 µmol L−1; open symbols) or with N2 only (closed symbols). *Calculated NO3− concentrations (see Methods section for details). Error bars represent standard deviations on means from 3 culture replicates.
Mentions: In high-light-acclimated cultures, long-term exposure to 30 µM NO3− yielded significantly higher growth rates (µ = 0.87 d−1) than those in control cultures without added NO3− (µ = 0.68 d−1; p<0.05), indicating that growth was limited by the N2-assimilation rate (Fig. 2a). Diminishing NO3− concentrations over time suggested that NO3−-assimilation rates in fast-growing cultures (µ = 0.87 d−1) were 2.8 times higher than those in slow-growing cultures (µ = 0.23 d−1; Fig. 3a; p<0.05), but the contribution of NO3− to the total daily N assimilation still varied as a function of growth rate. In high-light-acclimated cultures exposed to NO3− (µ = 0.87 d−1), NO3− assimilation represented 40% of the total daily N assimilation while N2 assimilation represented 60% (Fig. 2b). When combined, NO3− and N2 assimilation yielded a higher total daily N-assimilation rate (187 fmol N cell−1 d−1) than that in the control treatment growing on N2 only (122 fmol N cell−1 d−1; p<0.05; Fig. 2b). Furthermore, N2-fixation rates in cultures with added NO3− were not significantly different than those in control cultures without NO3− (p<0.05; Fig. 2b).

Bottom Line: In high-light-acclimated, fast-growing cultures, NO3- did not inhibit N2-fixation rates in comparison with cultures growing on N2 alone.Instead NO3- supported even faster growth, indicating that the cellular assimilation rate of N2 alone (i.e. dinitrogen reduction) could not support the light-specific maximum growth rate of Crocosphaera.When growth was severely light-limited, NO3- did not support faster growth rates but instead inhibited N2-fixation rates by 55% relative to controls.

View Article: PubMed Central - PubMed

Affiliation: Marine and Environmental Biology, Department of Biological Sciences, University of Southern California, Los Angeles, CA, United States of America.

ABSTRACT
Biological N2 fixation is the dominant supply of new nitrogen (N) to the oceans, but is often inhibited in the presence of fixed N sources such as nitrate (NO3-). Anthropogenic fixed N inputs to the ocean are increasing, but their effect on marine N2 fixation is uncertain. Thus, global estimates of new oceanic N depend on a fundamental understanding of factors that modulate N source preferences by N2-fixing cyanobacteria. We examined the unicellular diazotroph Crocosphaera watsonii (strain WH0003) to determine how the light-limited growth rate influences the inhibitory effects of fixed N on N2 fixation. When growth (µ) was limited by low light (µ = 0.23 d-1), short-term experiments indicated that 0.4 µM NH4+ reduced N2-fixation by ∼90% relative to controls without added NH4+. In fast-growing, high-light-acclimated cultures (µ = 0.68 d-1), 2.0 µM NH4+ was needed to achieve the same effect. In long-term exposures to NO3-, inhibition of N2 fixation also varied with growth rate. In high-light-acclimated, fast-growing cultures, NO3- did not inhibit N2-fixation rates in comparison with cultures growing on N2 alone. Instead NO3- supported even faster growth, indicating that the cellular assimilation rate of N2 alone (i.e. dinitrogen reduction) could not support the light-specific maximum growth rate of Crocosphaera. When growth was severely light-limited, NO3- did not support faster growth rates but instead inhibited N2-fixation rates by 55% relative to controls. These data rest on the basic tenet that light energy is the driver of photoautotrophic growth while various nutrient substrates serve as supports. Our findings provide a novel conceptual framework to examine interactions between N source preferences and predict degrees of inhibition of N2 fixation by fixed N sources based on the growth rate as controlled by light.

Show MeSH
Related in: MedlinePlus