A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii

Nitrogen fixation is advantageous in microbial competition when bioavailable nitrogen is scarce, but has substantial costs for growth rate and growth efficiency. To quantify these costs, we have developed a model of a nitrogen-fixing bacterium that constrains mass, electron and energy flow at the sc...

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Main Authors: Bragg, Jason, Follows, Michael J
Other Authors: Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Format: Article
Published: Nature Publishing Group 2018
Online Access:http://hdl.handle.net/1721.1/118428
https://orcid.org/0000-0002-3102-0341
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author Bragg, Jason
Follows, Michael J
author2 Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
author_facet Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Bragg, Jason
Follows, Michael J
author_sort Bragg, Jason
collection MIT
description Nitrogen fixation is advantageous in microbial competition when bioavailable nitrogen is scarce, but has substantial costs for growth rate and growth efficiency. To quantify these costs, we have developed a model of a nitrogen-fixing bacterium that constrains mass, electron and energy flow at the scale of the individual. When tested and calibrated with laboratory data for the soil bacterium Azotobacter vinelandii, the model reveals that the direct energetic cost of nitrogen fixation is small relative to the cost of managing intracellular oxygen. It quantifies the costs and benefits of several potential oxygen protection mechanisms present in nature including enhanced respiration (respiratory protection) as well as the production of extracellular polymers as a barrier to O₂ diffusion, and increasing cell size. The latter mechanisms lead to higher growth efficiencies relative to respiratory protection alone. This simple, yet mechanistic framework provides a quantitative model of nitrogen fixation, which can be applied in ecological simulations.
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spelling mit-1721.1/1184282022-09-30T00:06:10Z A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii Bragg, Jason Follows, Michael J Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Follows, Michael J Nitrogen fixation is advantageous in microbial competition when bioavailable nitrogen is scarce, but has substantial costs for growth rate and growth efficiency. To quantify these costs, we have developed a model of a nitrogen-fixing bacterium that constrains mass, electron and energy flow at the scale of the individual. When tested and calibrated with laboratory data for the soil bacterium Azotobacter vinelandii, the model reveals that the direct energetic cost of nitrogen fixation is small relative to the cost of managing intracellular oxygen. It quantifies the costs and benefits of several potential oxygen protection mechanisms present in nature including enhanced respiration (respiratory protection) as well as the production of extracellular polymers as a barrier to O₂ diffusion, and increasing cell size. The latter mechanisms lead to higher growth efficiencies relative to respiratory protection alone. This simple, yet mechanistic framework provides a quantitative model of nitrogen fixation, which can be applied in ecological simulations. Gordon and Betty Moore Foundation (Grant GBMF3778) Simons Foundation (Award 329108) 2018-10-11T14:58:01Z 2018-10-11T14:58:01Z 2016-10 2016-06 2018-09-24T17:22:21Z Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 http://hdl.handle.net/1721.1/118428 Inomura, Keisuke et al. “A Quantitative Analysis of the Direct and Indirect Costs of Nitrogen Fixation: a Model Based on Azotobacter Vinelandii.” The ISME Journal 11, 1 (October 2016): 166–175 © 2017 International Society for Microbial Ecology https://orcid.org/0000-0002-3102-0341 http://dx.doi.org/10.1038/ISMEJ.2016.97 ISME Journal Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Nature Publishing Group Nature
spellingShingle Bragg, Jason
Follows, Michael J
A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii
title A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii
title_full A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii
title_fullStr A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii
title_full_unstemmed A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii
title_short A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii
title_sort quantitative analysis of the direct and indirect costs of nitrogen fixation a model based on azotobacter vinelandii
url http://hdl.handle.net/1721.1/118428
https://orcid.org/0000-0002-3102-0341
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