Anaerobic nitrate respiration in the aerobe Streptomyces coelicolor A3(2): helping maintain a proton gradient during dormancy.

Abstract

Respiratory nitrate reductases (Nar) catalyse the reduction of nitrate to nitrite, coupling this process to energy conservation. The obligate aerobic actinobacterium Streptomyces coelicolor synthesizes three Nar enzymes that contribute to maintenance of a membrane potential when either the mycelium or the spores become hypoxic or anoxic. No growth occurs under such conditions but the bacterium survives the lack of O2 by remaining metabolically active; reducing nitrate is one means whereby this process is aided. Nar1 is exclusive to spores, Nar2 to vegetative mycelium and Nar3 to stationary-phase mycelium, each making a distinct contribution to energy conservation. While Nar2 and Nar3 appear to function like conventional menaquinol oxidases, unusually, Nar1 is completely dependent for its activity on a cytochrome bcc-aa 3 oxidase supercomplex. This suggest that electrons within this supercomplex are diverted to Nar1 during O2 limitation. Receiving electrons from this supercomplex potentially allows nitrate reduction to be coupled to the Q-cycle of the cytochrome bcc complex. This modification likely improves the efficiency of energy conservation, extending longevity of spores under O2 limitation. Knowledge gained on the bioenergetics of NO3 - respiration in the actinobacteria will aid our understanding of how many microorganisms survive under conditions of extreme nutrient and energy restriction.