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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.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'.

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'.

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Modelling of (h−1) as a function of .A. The panel shows the O2 concentration in the liquid-phase  falling as a result of aerobic respiration. B. The panel shows the probability for a cell to switch to denitrification (, h−1) modelled as a function of .  (Panels A & B) is the concentration below which  is assumed to trigger (due to withdrawal of the transcriptional control of O2 on denitrification [22]), whereas  is assumed to be the concentration below which  terminates (due to lack of energy for enzyme synthesis). The double-headed arrow (at the bottom of Panel A) illustrates the limited time-window () available for the cells to switch to denitrification.
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pcbi-1003933-g005: Modelling of (h−1) as a function of .A. The panel shows the O2 concentration in the liquid-phase falling as a result of aerobic respiration. B. The panel shows the probability for a cell to switch to denitrification (, h−1) modelled as a function of . (Panels A & B) is the concentration below which is assumed to trigger (due to withdrawal of the transcriptional control of O2 on denitrification [22]), whereas is assumed to be the concentration below which terminates (due to lack of energy for enzyme synthesis). The double-headed arrow (at the bottom of Panel A) illustrates the limited time-window () available for the cells to switch to denitrification.

Mentions: where (h−1) represents the conditional specific-probability for any cell to be recruited to denitrification, modelled as a function of O2 concentration in the liquid-phase (, see Fig. 5):(8)


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)

Modelling of (h−1) as a function of .A. The panel shows the O2 concentration in the liquid-phase  falling as a result of aerobic respiration. B. The panel shows the probability for a cell to switch to denitrification (, h−1) modelled as a function of .  (Panels A & B) is the concentration below which  is assumed to trigger (due to withdrawal of the transcriptional control of O2 on denitrification [22]), whereas  is assumed to be the concentration below which  terminates (due to lack of energy for enzyme synthesis). The double-headed arrow (at the bottom of Panel A) illustrates the limited time-window () available for the cells to switch to denitrification.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003933-g005: Modelling of (h−1) as a function of .A. The panel shows the O2 concentration in the liquid-phase falling as a result of aerobic respiration. B. The panel shows the probability for a cell to switch to denitrification (, h−1) modelled as a function of . (Panels A & B) is the concentration below which is assumed to trigger (due to withdrawal of the transcriptional control of O2 on denitrification [22]), whereas is assumed to be the concentration below which terminates (due to lack of energy for enzyme synthesis). The double-headed arrow (at the bottom of Panel A) illustrates the limited time-window () available for the cells to switch to denitrification.
Mentions: where (h−1) represents the conditional specific-probability for any cell to be recruited to denitrification, modelled as a function of O2 concentration in the liquid-phase (, see Fig. 5):(8)

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.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'.

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