Oxygen-Dependent Control of Respiratory Nitrate Reduction in Mycelium of Streptomyces coelicolor A3(2)

Abstract

Several members of the obligately aerobic genus Streptomyces are able to reduce nitrate, catalyzed by Nar-type respiratory nitrate reductases. A unique feature of Streptomyces coelicolor A3(2) compared with other streptomycetes is that it synthesizes three nonredundant Nar enzymes. In this study, we show that Nar2 is the main Nar enzyme active in mycelium and could characterize the conditions governing its synthesis. Nar2 was present at low levels in aerobically cultivated mycelium, but synthesis was induced when cultures were grown under oxygen limitation. Growth in the presence of high oxygen concentrations prevented the induction of Nar2 synthesis. Equally, an abrupt shift from aerobiosis to anaerobiosis did not result in the immediate induction of Nar2 synthesis. This suggests that the synthesis of Nar2 is induced during a hypoxic downshift, probably to allow maintenance of a proton gradient during the transition to anaerobiosis. Although no Nar2 could be detected in freshly harvested mature spores, synthesis of the enzyme could be induced after long-term (several days) incubation of these resting spores under anaerobic conditions. Induction of Nar2 synthesis in spores was linked to transcriptional control. Nar2 activity in whole mycelium was strictly dependent on the presence of a putative nitrate transporter, NarK2. The oxygen-dependent inhibition of nitrate reduction by Nar2 was mediated by NarK2-dependent nitrate:nitrite antiport. This antiport mechanism likely prevents the accumulation of toxic nitrite in the cytoplasm. A deletion of the narK2 gene had no effect on Nar1-dependent nitrate reduction in resting spores. Together, our results indicate redox-dependent transcriptional and posttranslational control of nitrate reduction by Nar2.

Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27

“…The transcriptomics and proteomics data in the study suggested that N. eutropha strain C91 tuned down the assimilatory metabolism while retaining or stimulating dissimilatory metabolism upon anoxic incubation with NO 2 as the surrogate oxidant. A Grampositive obligate aerobic bacterium, Streptomyces coelicolor A3(2), was also found to utilize its Nar-type respiratory nitrate reductase to survive extended periods of anoxia, although no growth was observed in the absence of O 2 (36,37). The utilization of N 2 O as a temporary substitute for O 2 in G. aurantiaca strain T-27 may be another such lifestyle that strictly aerobic microorganisms have adopted to generate cell maintenance energy to survive through periods of anoxia.…”

Cytochrome <b><i>bcc-aa3</i></b> Oxidase Supercomplexes in the Aerobic Respiratory Chain of <b><i>Streptomyces coelicolor</i></b> A3(2)

“…Growth of S. coelicolor A3(2) strains as highly dispersed liquid cultures in Duran-F tubes with MOPS-buffered TSB was performed as described [Fischer et al, 2014]. Standardized 15-h exponential cultures (20 mL) were inoculated with 2 mL of a standard mycelium suspension.…”

Response of microbial community function to fluctuating geochemical conditions within a legacy radioactive waste trench environment

“…The inorganic nitrogen cycling results provide important information regarding the transition from aerobic to anaerobic conditions as the water level declines. The competing requirements of nitrate respiration, which necessitates oxygen-limiting conditions at a minimum (61), and NO dioxygenase needing molecular oxygen, collectively suggest that at day 4 the trench waters were no longer aerobic, but more likely microaerophilic/hypoxic. However, many facultative anaerobes are capable of using nitrate as an alternate electron acceptor when oxygen is not available.…”