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

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 ( (Formula presented.) ). 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 ( (Formula presented.) , 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 (Formula presented.)  = 0.005 h−1, the model robustly simulates observed denitrification kinetics for a range of culture conditions. The resulting (Formula presented.) (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’.