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

Regulated Stochasticity in a Bacterial Signaling Network Permits Tolerance to a Rapid Environmental Change

“…This evolutionary strategy, called bet hedging, enables a population to prepare for a potential switch to a new environmental condition by harboring a subpopulation that is pre-adapted to the new environment. Bet hedging has been characterized in a number of microbial systems and shown to play a role in many processes, including pathogenesis (Ackermann et al, 2008; Stewart and Cookson, 2012), antibiotic persistence (Balaban et al, 2004; Maisonneuve and Gerdes, 2014; Verstraeten et al, 2015; Wakamoto et al, 2013), cellular differentiation (Veening et al, 2008b), regulation of metabolism (Hassan et al, 2014; Kotte et al, 2014; Ratcliff and Denison, 2010), induction of stress responses (Sureka et al, 2008), and viral latency (Maslov and Sneppen, 2015; Rouzine et al, 2015). Stochasticity in gene expression is often responsible for the generation of phenotypic diversity in these systems and frequently results in a bimodal distribution of phenotypes (Kotte et al, 2014; Nielsen et al, 2010; Ozbudak et al, 2004; Veening et al, 2008b), although bimodality is not always observed (El Meouche et al, 2016; Levy et al, 2012).…”

Denitrifying haloarchaea within the genus Haloferax display divergent respiratory phenotypes, with implications for their release of nitrogenous gases

“…In other denitrifiers, similar gas kinetics have been taken to suggest that only a small fraction of cells synthesize the core denitrification enzymes and then grow exponentially. This phenomenon has been explored by modelling and experiments in the α‐proteobacterium P. denitrificans , where a low probability of nirS expression and high probability of nar expression results in nitrite accumulation, followed by its reduction by a minority of NIR positive cells (Hassan et al, ; ; Lycus et al, ). In H. denitrificans , there is no significant accumulation of nitrite, thus, the gatekeeper appears to be NAR.…”

Modularity of nitrogen‐oxide reducing soil bacteria: linking phenotype to genotype

“…S5, S7, S8 and S10). By plotting , and ( + ) against time, we were able to inspect if the transition from aerobic to anaerobic respiration resulted in a long lasting depression of respiratory metabolism, as observed in similar experiments with Paracoccus denitrificans (Bergaust et al , ; Hassan et al , ).…”