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

Abstract

Summary 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.

Coelimycin Synthesis Activatory Proteins Are Key Regulators of Specialized Metabolism and Precursor Flux in Streptomyces coelicolor A3(2)

“…Streptomyces life cycle involves formation of a dense vegetative mycelium which may locally experience hypoxia (Sawers et al, 2019). An early, compartmentalized mycelium (MI) is transformed to a multinucleated substrate mycelium (MII without the hydrophobic layer) which starts specialized metabolite synthesis and further develops into aerial mycelium (MII with a hydrophobic layer) and into spore chains (Yagüe et al, 2013).…”

The Potential for Redox-Active Metabolites To Enhance or Unlock Anaerobic Survival Metabolisms in Aerobes

“…coelicolor, where nitrate reduction can occur simultaneously with oxygen (83). While it is unclear why nitrate reduction is insufficient to support anaerobic growth of S. coelicolor, it has been inferred that nitrate reduction contributes to charging the PMF and/or redox-balancing the cytosol in the absence of oxygen to contribute to cell survival (85). For a detailed summary and analysis of denitrification in S. coelicolor, please see the recent review by Sawers et al (85).…”

Circulating metabolomics profiling reveals novel pathways associated with cognitive decline in patients with hypertension

“…In the nitrite ammonification processes, nitrite was converted to ammonia through the reaction equations 1-4. 51 Nitrate respiration processes proceed by using nitrate as an electron acceptor at low oxygen concentrations resulting in the production of dinitrogen. The absence of the microbes with ammonia oxidation and nitrite oxidation functions confirms that these microbes dwelled in anaerobic conditions, for example, in the gut.…”