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Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification

In response to impending anoxic conditions, denitrifying bacteria sustain respiratory metabolism by producing enzymes for reducing nitrogen oxyanions/-oxides (NO(x)) to N(2) (denitrification). Since denitrifying bacteria are non-fermentative, the initial production of denitrification proteome depend...

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Autores principales: Hassan, Junaid, Bergaust, Linda L., Wheat, I. David, Bakken, Lars R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4222654/
https://www.ncbi.nlm.nih.gov/pubmed/25375393
http://dx.doi.org/10.1371/journal.pcbi.1003933
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author Hassan, Junaid
Bergaust, Linda L.
Wheat, I. David
Bakken, Lars R.
author_facet Hassan, Junaid
Bergaust, Linda L.
Wheat, I. David
Bakken, Lars R.
author_sort Hassan, Junaid
collection PubMed
description In response to impending anoxic conditions, denitrifying bacteria sustain respiratory metabolism by producing enzymes for reducing nitrogen oxyanions/-oxides (NO(x)) to N(2) (denitrification). Since denitrifying bacteria are non-fermentative, the initial production of denitrification proteome depends on energy from aerobic respiration. Thus, if a cell fails to synthesise a minimum of denitrification proteome before O(2) is completely exhausted, it will be unable to produce it later due to energy-limitation. Such entrapment in anoxia is recently claimed to be a major phenomenon in batch cultures of the model organism Paracoccus denitrificans on the basis of measured e(−)-flow rates to O(2) and NO(x). Here we constructed a dynamic model and explicitly simulated actual kinetics of recruitment of the cells to denitrification to directly and more accurately estimate the recruited fraction ([Image: see text]). Transcription of nirS is pivotal for denitrification, for it triggers a cascade of events leading to the synthesis of a full-fledged denitrification proteome. The model is based on the hypothesis that nirS has a low probability ([Image: see text], h(−1)) of initial transcription, but once initiated, the transcription is greatly enhanced through positive feedback by NO, resulting in the recruitment of the transcribing cell to denitrification. We assume that the recruitment is initiated as [O(2)] falls below a critical threshold and terminates (assuming energy-limitation) as [O(2)] exhausts. With [Image: see text] = 0.005 h(−1), the model robustly simulates observed denitrification kinetics for a range of culture conditions. The resulting [Image: see text] (fraction of the cells recruited to denitrification) falls within 0.038–0.161. In contrast, if the recruitment of the entire population is assumed, the simulated denitrification kinetics deviate grossly from those observed. The phenomenon can be understood as a ‘bet-hedging strategy’: switching to denitrification is a gain if anoxic spell lasts long but is a waste of energy if anoxia turns out to be a ‘false alarm’.
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spelling pubmed-42226542014-11-13 Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification Hassan, Junaid Bergaust, Linda L. Wheat, I. David Bakken, Lars R. PLoS Comput Biol Research Article In response to impending anoxic conditions, denitrifying bacteria sustain respiratory metabolism by producing enzymes for reducing nitrogen oxyanions/-oxides (NO(x)) to N(2) (denitrification). Since denitrifying bacteria are non-fermentative, the initial production of denitrification proteome depends on energy from aerobic respiration. Thus, if a cell fails to synthesise a minimum of denitrification proteome before O(2) is completely exhausted, it will be unable to produce it later due to energy-limitation. Such entrapment in anoxia is recently claimed to be a major phenomenon in batch cultures of the model organism Paracoccus denitrificans on the basis of measured e(−)-flow rates to O(2) and NO(x). Here we constructed a dynamic model and explicitly simulated actual kinetics of recruitment of the cells to denitrification to directly and more accurately estimate the recruited fraction ([Image: see text]). Transcription of nirS is pivotal for denitrification, for it triggers a cascade of events leading to the synthesis of a full-fledged denitrification proteome. The model is based on the hypothesis that nirS has a low probability ([Image: see text], h(−1)) of initial transcription, but once initiated, the transcription is greatly enhanced through positive feedback by NO, resulting in the recruitment of the transcribing cell to denitrification. We assume that the recruitment is initiated as [O(2)] falls below a critical threshold and terminates (assuming energy-limitation) as [O(2)] exhausts. With [Image: see text] = 0.005 h(−1), the model robustly simulates observed denitrification kinetics for a range of culture conditions. The resulting [Image: see text] (fraction of the cells recruited to denitrification) falls within 0.038–0.161. In contrast, if the recruitment of the entire population is assumed, the simulated denitrification kinetics deviate grossly from those observed. The phenomenon can be understood as a ‘bet-hedging strategy’: switching to denitrification is a gain if anoxic spell lasts long but is a waste of energy if anoxia turns out to be a ‘false alarm’. Public Library of Science 2014-11-06 /pmc/articles/PMC4222654/ /pubmed/25375393 http://dx.doi.org/10.1371/journal.pcbi.1003933 Text en © 2014 Hassan et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Hassan, Junaid
Bergaust, Linda L.
Wheat, I. David
Bakken, Lars R.
Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification
title Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification
title_full Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification
title_fullStr Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification
title_full_unstemmed Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification
title_short Low Probability of Initiating nirS Transcription Explains Observed Gas Kinetics and Growth of Bacteria Switching from Aerobic Respiration to Denitrification
title_sort low probability of initiating nirs transcription explains observed gas kinetics and growth of bacteria switching from aerobic respiration to denitrification
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4222654/
https://www.ncbi.nlm.nih.gov/pubmed/25375393
http://dx.doi.org/10.1371/journal.pcbi.1003933
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