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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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Related in: MedlinePlus

Growth-specific assimilation rates of nitrate (NO3−; open bars) and dinitrogen (N2; closed bars) in cultures of C. watsonii (WH0003) with added NO3− (30 µmol L−1).Growth-specific NO3− and N2-assimilation rates change inversely relative to each other as a function of light-limited growth. Error bars represent standard deviations on means from 3 culture replicates.
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pone-0114465-g004: Growth-specific assimilation rates of nitrate (NO3−; open bars) and dinitrogen (N2; closed bars) in cultures of C. watsonii (WH0003) with added NO3− (30 µmol L−1).Growth-specific NO3− and N2-assimilation rates change inversely relative to each other as a function of light-limited growth. Error bars represent standard deviations on means from 3 culture replicates.

Mentions: Under low light, long-term exposure to 30 µM NO3− did not support faster growth rates (Fig. 2a, 3b) even though NO3−-uptake supported 61% of the total daily N assimilation. Instead, N2-fixation rates were reduced by 55% relative to those in cultures without added NO3− (p<0.05; Fig. 2a). Thus, in cultures that were grown with NO3−, there was a clear shift in the ratio of N source utilization where growth-specific NO3−-assimilation rates increased by 55% with decreasing light,while growth-specific N2-assimilation rates increased by 46% with increasing light (Fig. 4). In both the high- and low-light treatments with 30 µM NO3− added, the concentration of NO3− was high (>16 µmol NO3− L−1) throughout the entire 66 h or 114 h sampling period (Fig. 3).


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

Garcia NS, Hutchins DA - PLoS ONE (2014)

Growth-specific assimilation rates of nitrate (NO3−; open bars) and dinitrogen (N2; closed bars) in cultures of C. watsonii (WH0003) with added NO3− (30 µmol L−1).Growth-specific NO3− and N2-assimilation rates change inversely relative to each other as a function of light-limited growth. 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-g004: Growth-specific assimilation rates of nitrate (NO3−; open bars) and dinitrogen (N2; closed bars) in cultures of C. watsonii (WH0003) with added NO3− (30 µmol L−1).Growth-specific NO3− and N2-assimilation rates change inversely relative to each other as a function of light-limited growth. Error bars represent standard deviations on means from 3 culture replicates.
Mentions: Under low light, long-term exposure to 30 µM NO3− did not support faster growth rates (Fig. 2a, 3b) even though NO3−-uptake supported 61% of the total daily N assimilation. Instead, N2-fixation rates were reduced by 55% relative to those in cultures without added NO3− (p<0.05; Fig. 2a). Thus, in cultures that were grown with NO3−, there was a clear shift in the ratio of N source utilization where growth-specific NO3−-assimilation rates increased by 55% with decreasing light,while growth-specific N2-assimilation rates increased by 46% with increasing light (Fig. 4). In both the high- and low-light treatments with 30 µM NO3− added, the concentration of NO3− was high (>16 µmol NO3− L−1) throughout the entire 66 h or 114 h sampling period (Fig. 3).

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