Limits...
Low probability of initiating nirS transcription explains observed gas kinetics and growth of bacteria switching from aerobic respiration to denitrification.

Hassan J, Bergaust LL, Wheat ID, Bakken LR - PLoS Comput. Biol. (2014)

Bottom Line: The model is based on the hypothesis that nirS has a low probability (rden, 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.The resulting Fden (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.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Sciences, Norwegian University of Life Sciences, Ås, Norway.

ABSTRACT
In response to impending anoxic conditions, denitrifying bacteria sustain respiratory metabolism by producing enzymes for reducing nitrogen oxyanions/-oxides (NOx) to N2 (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 O2 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 O2 and NOx. 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 (Fden). 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 (rden, 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 [O2] falls below a critical threshold and terminates (assuming energy-limitation) as [O2] exhausts. With rden = 0.005 h(-1), the model robustly simulates observed denitrification kinetics for a range of culture conditions. The resulting Fden (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'.

Show MeSH

Related in: MedlinePlus

Sensitivity analysis (1): Varying initial O2 in the headspace  within a low range.The figure shows the impact of varying  within a low range on: A. O2 concentration in the liquid-phase , B. The number of aerobically growing cells (), which do not possess denitrification enzymes, C. The rate of recruitment of  to denitrification (), and D. N2 accumulation. Marked in Panel A,  is the  below which  triggers, and  is the  below which  terminates. In Panel C, the spikes of recruitment (following the initial recruitment) are due to spikes of O2 by sampling, causing  to transiently exceed . The model predicts that reducing  within a low range (Panel A) will lower the number of aerobically grown cells (Panel B) and, thereby, the recruitment rate (Panel C), thus increasing the time taken to deplete  (slower N2 accumulation, Panel D).
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4222654&req=5

pcbi-1003933-g011: Sensitivity analysis (1): Varying initial O2 in the headspace within a low range.The figure shows the impact of varying within a low range on: A. O2 concentration in the liquid-phase , B. The number of aerobically growing cells (), which do not possess denitrification enzymes, C. The rate of recruitment of to denitrification (), and D. N2 accumulation. Marked in Panel A, is the below which triggers, and is the below which terminates. In Panel C, the spikes of recruitment (following the initial recruitment) are due to spikes of O2 by sampling, causing to transiently exceed . The model predicts that reducing within a low range (Panel A) will lower the number of aerobically grown cells (Panel B) and, thereby, the recruitment rate (Panel C), thus increasing the time taken to deplete (slower N2 accumulation, Panel D).

Mentions: This is rather a simple case demonstrating that increasing within this low range (Fig. 11A) will result in increasing rates of denitrification (Fig. 11D) by increasing the number of aerobically grown cells (, Fig. 11B) and, thus, the rate of recruitment (, Fig. 11C).


Low probability of initiating nirS transcription explains observed gas kinetics and growth of bacteria switching from aerobic respiration to denitrification.

Hassan J, Bergaust LL, Wheat ID, Bakken LR - PLoS Comput. Biol. (2014)

Sensitivity analysis (1): Varying initial O2 in the headspace  within a low range.The figure shows the impact of varying  within a low range on: A. O2 concentration in the liquid-phase , B. The number of aerobically growing cells (), which do not possess denitrification enzymes, C. The rate of recruitment of  to denitrification (), and D. N2 accumulation. Marked in Panel A,  is the  below which  triggers, and  is the  below which  terminates. In Panel C, the spikes of recruitment (following the initial recruitment) are due to spikes of O2 by sampling, causing  to transiently exceed . The model predicts that reducing  within a low range (Panel A) will lower the number of aerobically grown cells (Panel B) and, thereby, the recruitment rate (Panel C), thus increasing the time taken to deplete  (slower N2 accumulation, Panel D).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4222654&req=5

pcbi-1003933-g011: Sensitivity analysis (1): Varying initial O2 in the headspace within a low range.The figure shows the impact of varying within a low range on: A. O2 concentration in the liquid-phase , B. The number of aerobically growing cells (), which do not possess denitrification enzymes, C. The rate of recruitment of to denitrification (), and D. N2 accumulation. Marked in Panel A, is the below which triggers, and is the below which terminates. In Panel C, the spikes of recruitment (following the initial recruitment) are due to spikes of O2 by sampling, causing to transiently exceed . The model predicts that reducing within a low range (Panel A) will lower the number of aerobically grown cells (Panel B) and, thereby, the recruitment rate (Panel C), thus increasing the time taken to deplete (slower N2 accumulation, Panel D).
Mentions: This is rather a simple case demonstrating that increasing within this low range (Fig. 11A) will result in increasing rates of denitrification (Fig. 11D) by increasing the number of aerobically grown cells (, Fig. 11B) and, thus, the rate of recruitment (, Fig. 11C).

Bottom Line: The model is based on the hypothesis that nirS has a low probability (rden, 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.The resulting Fden (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.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Sciences, Norwegian University of Life Sciences, Ås, Norway.

ABSTRACT
In response to impending anoxic conditions, denitrifying bacteria sustain respiratory metabolism by producing enzymes for reducing nitrogen oxyanions/-oxides (NOx) to N2 (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 O2 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 O2 and NOx. 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 (Fden). 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 (rden, 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 [O2] falls below a critical threshold and terminates (assuming energy-limitation) as [O2] exhausts. With rden = 0.005 h(-1), the model robustly simulates observed denitrification kinetics for a range of culture conditions. The resulting Fden (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'.

Show MeSH
Related in: MedlinePlus