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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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Short-term inhibitory effects of ammonium (NH4+, 0–1.5 µmol L−1) and nitrate (NO3−, 0–40 µmol L−1) on N2 fixation by Crocosphaera watsonii (WH0003) (percent of control with no added nitrogen).Cultures were grown in steady state under high light (175 µmol quanta m−2 s−1, growth rate (µ) = 0.68 d−1, open symbols) and low light (25 µmol quanta m−2 s−1, µ = 0.23 d−1, closed symbols) before adding nitrogen. Error bars represent standard deviations on means from 3 culture replicates.
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pone-0114465-g001: Short-term inhibitory effects of ammonium (NH4+, 0–1.5 µmol L−1) and nitrate (NO3−, 0–40 µmol L−1) on N2 fixation by Crocosphaera watsonii (WH0003) (percent of control with no added nitrogen).Cultures were grown in steady state under high light (175 µmol quanta m−2 s−1, growth rate (µ) = 0.68 d−1, open symbols) and low light (25 µmol quanta m−2 s−1, µ = 0.23 d−1, closed symbols) before adding nitrogen. Error bars represent standard deviations on means from 3 culture replicates.

Mentions: In slow-growing cultures acclimated to low light, short-term additions of 0.4 µM NH4+ inhibited N2-fixation rates to <10% of rates in control treatments without added NH4+ (Fig. 1a). In faster-growing cultures acclimated to 175 µmol quanta m−2 s−1, with biomass concentrations equivalent to those in low-light cultures (Table 1), short-term exposure to five times as much NH4+ (2.0 µM) was needed to achieve the same inhibitory effect on N2 fixation (Fig. 1a). The short-term inhibitory effects of NO3− on N2 fixation also varied as a function of growth rate. In slow-growing, low-light acclimated cultures, short-term exposure to NO3− reduced mean N2-fixation rates by ∼47–62% relative to rates in control treatments without added NO3− (Fig. 1b). In fast-growing cultures acclimated to high light, however, short-term additions of NO3− at any concentration up to 40 µM did not inhibit mean N2-fixation rates by more than 9%, relative to N2-fixation rates in control cultures without added NO3− (Fig. 1b).


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

Garcia NS, Hutchins DA - PLoS ONE (2014)

Short-term inhibitory effects of ammonium (NH4+, 0–1.5 µmol L−1) and nitrate (NO3−, 0–40 µmol L−1) on N2 fixation by Crocosphaera watsonii (WH0003) (percent of control with no added nitrogen).Cultures were grown in steady state under high light (175 µmol quanta m−2 s−1, growth rate (µ) = 0.68 d−1, open symbols) and low light (25 µmol quanta m−2 s−1, µ = 0.23 d−1, closed symbols) before adding nitrogen. 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-g001: Short-term inhibitory effects of ammonium (NH4+, 0–1.5 µmol L−1) and nitrate (NO3−, 0–40 µmol L−1) on N2 fixation by Crocosphaera watsonii (WH0003) (percent of control with no added nitrogen).Cultures were grown in steady state under high light (175 µmol quanta m−2 s−1, growth rate (µ) = 0.68 d−1, open symbols) and low light (25 µmol quanta m−2 s−1, µ = 0.23 d−1, closed symbols) before adding nitrogen. Error bars represent standard deviations on means from 3 culture replicates.
Mentions: In slow-growing cultures acclimated to low light, short-term additions of 0.4 µM NH4+ inhibited N2-fixation rates to <10% of rates in control treatments without added NH4+ (Fig. 1a). In faster-growing cultures acclimated to 175 µmol quanta m−2 s−1, with biomass concentrations equivalent to those in low-light cultures (Table 1), short-term exposure to five times as much NH4+ (2.0 µM) was needed to achieve the same inhibitory effect on N2 fixation (Fig. 1a). The short-term inhibitory effects of NO3− on N2 fixation also varied as a function of growth rate. In slow-growing, low-light acclimated cultures, short-term exposure to NO3− reduced mean N2-fixation rates by ∼47–62% relative to rates in control treatments without added NO3− (Fig. 1b). In fast-growing cultures acclimated to high light, however, short-term additions of NO3− at any concentration up to 40 µM did not inhibit mean N2-fixation rates by more than 9%, relative to N2-fixation rates in control cultures without added NO3− (Fig. 1b).

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