Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium

Denitrifying microbes sequentially reduce nitrate (NO₃⁻) to nitrite (NO₂⁻), NO, N₂O, and N₂ through enzymes encoded by nar, nir, nor, and nos. Some denitrifiers maintain the whole four-gene pathway, but others possess partial pathways. Partial denitrifiers may evolve through metabolic specialization...

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Main Authors: Zhang, Irene H., Mullen, Susan, Ciccarese, Davide, Dumit, Diana, Martocello, Donald E., Toyofuku, Masanori, Nomura, Nobuhiko, Smriga, Steven, Babbin, Andrew R.
Other Authors: Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Format: Article
Language:English
Published: Frontiers Media SA 2021
Online Access:https://hdl.handle.net/1721.1/133133
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author Zhang, Irene H.
Mullen, Susan
Ciccarese, Davide
Dumit, Diana
Martocello, Donald E.
Toyofuku, Masanori
Nomura, Nobuhiko
Smriga, Steven
Babbin, Andrew R.
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
Zhang, Irene H.
Mullen, Susan
Ciccarese, Davide
Dumit, Diana
Martocello, Donald E.
Toyofuku, Masanori
Nomura, Nobuhiko
Smriga, Steven
Babbin, Andrew R.
author_sort Zhang, Irene H.
collection MIT
description Denitrifying microbes sequentially reduce nitrate (NO₃⁻) to nitrite (NO₂⁻), NO, N₂O, and N₂ through enzymes encoded by nar, nir, nor, and nos. Some denitrifiers maintain the whole four-gene pathway, but others possess partial pathways. Partial denitrifiers may evolve through metabolic specialization whereas complete denitrifiers may adapt toward greater metabolic flexibility in nitrogen oxide (NO[subscript x]⁻) utilization. Both exist within natural environments, but we lack an understanding of selective pressures driving the evolution toward each lifestyle. Here we investigate differences in growth rate, growth yield, denitrification dynamics, and the extent of intermediate metabolite accumulation under varying nutrient conditions between the model complete denitrifier Pseudomonas aeruginosa and a community of engineered specialists with deletions in the denitrification genes nar or nir. Our results in a mixed carbon medium indicate a growth rate vs. yield tradeoff between complete and partial denitrifiers, which varies with total nutrient availability and ratios of organic carbon to NO[subscript x]⁻. We found that the cultures of both complete and partial denitrifiers accumulated nitrite and that the metabolic lifestyle coupled with nutrient conditions are responsible for the extent of nitrite accumulation.
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spelling mit-1721.1/1331332022-09-27T18:20:24Z Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium Zhang, Irene H. Mullen, Susan Ciccarese, Davide Dumit, Diana Martocello, Donald E. Toyofuku, Masanori Nomura, Nobuhiko Smriga, Steven Babbin, Andrew R. Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Massachusetts Institute of Technology. Microbiology Graduate Program Denitrifying microbes sequentially reduce nitrate (NO₃⁻) to nitrite (NO₂⁻), NO, N₂O, and N₂ through enzymes encoded by nar, nir, nor, and nos. Some denitrifiers maintain the whole four-gene pathway, but others possess partial pathways. Partial denitrifiers may evolve through metabolic specialization whereas complete denitrifiers may adapt toward greater metabolic flexibility in nitrogen oxide (NO[subscript x]⁻) utilization. Both exist within natural environments, but we lack an understanding of selective pressures driving the evolution toward each lifestyle. Here we investigate differences in growth rate, growth yield, denitrification dynamics, and the extent of intermediate metabolite accumulation under varying nutrient conditions between the model complete denitrifier Pseudomonas aeruginosa and a community of engineered specialists with deletions in the denitrification genes nar or nir. Our results in a mixed carbon medium indicate a growth rate vs. yield tradeoff between complete and partial denitrifiers, which varies with total nutrient availability and ratios of organic carbon to NO[subscript x]⁻. We found that the cultures of both complete and partial denitrifiers accumulated nitrite and that the metabolic lifestyle coupled with nutrient conditions are responsible for the extent of nitrite accumulation. Simons Foundation (Award 622065) 2021-10-26T18:01:01Z 2021-10-26T18:01:01Z 2021-09 2021-05 2021-10-26T16:30:26Z Article http://purl.org/eprint/type/JournalArticle 1664-302X https://hdl.handle.net/1721.1/133133 Zhang Irene H. et al. "Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium." Frontiers in Microbiology 12 (September 2021): 711073. © 2021 Zhang et al. en http://dx.doi.org/10.3389/fmicb.2021.711073 Frontiers in Microbiology Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Frontiers Media SA Frontiers
spellingShingle Zhang, Irene H.
Mullen, Susan
Ciccarese, Davide
Dumit, Diana
Martocello, Donald E.
Toyofuku, Masanori
Nomura, Nobuhiko
Smriga, Steven
Babbin, Andrew R.
Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium
title Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium
title_full Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium
title_fullStr Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium
title_full_unstemmed Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium
title_short Ratio of Electron Donor to Acceptor Influences Metabolic Specialization and Denitrification Dynamics in Pseudomonas aeruginosa in a Mixed Carbon Medium
title_sort ratio of electron donor to acceptor influences metabolic specialization and denitrification dynamics in pseudomonas aeruginosa in a mixed carbon medium
url https://hdl.handle.net/1721.1/133133
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