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

Abstract

N₂O-reducing organisms with nitrous oxide reductases (NosZ) are known as the only biological sink of N₂O in the environment. Among the most abundant <i>nosZ</i> genes found in the environment are <i>nosZ</i> genes affiliated with the understudied <i>Gemmatimonadetes</i> phylum. In this study, a unique regulatory mechanism of N₂O reduction in <i>Gemmatimonas aurantiaca</i> strain T-27, an isolate affiliated with the <i>Gemmatimonadetes</i> phylum, was examined. Strain T-27 was incubated with N₂O and/or O₂ as the electron acceptor. Significant N₂O reduction was observed only when O₂ was initially present. When batch cultures of strain T-27 were amended with O₂ and N₂O, N₂O reduction commenced after O₂ was depleted. In a long-term incubation with the addition of N₂O upon depletion, the N₂O reduction rate decreased over time and came to an eventual stop. Spiking of the culture with O₂ resulted in the resuscitation of N₂O reduction activity, supporting the hypothesis that N₂O reduction by strain T-27 required the transient presence of O₂ The highest level of <i>nosZ</i> transcription (8.97 <i>nosZ</i> transcripts/<i>recA</i> transcript) was observed immediately after O₂ depletion, and transcription decreased ∼25-fold within 85 h, supporting the observed phenotype. The observed difference between responses of strain T-27 cultures amended with and without N₂O to O₂ starvation suggested that N₂O helped sustain the viability of strain T-27 during temporary anoxia, although N₂O reduction was not coupled to growth. The findings in this study suggest that obligate aerobic microorganisms with <i>nosZ</i> genes may utilize N₂O as a temporary surrogate for O₂ to survive periodic anoxia.<b>IMPORTANCE</b> Emission of N₂O, a potent greenhouse gas and ozone depletion agent, from the soil environment is largely determined by microbial sources and sinks. N₂O reduction by organisms with N₂O reductases (NosZ) is the only known biological sink of N₂O at environmentally relevant concentrations (up to ∼1,000 parts per million by volume [ppmv]). Although a large fraction of <i>nosZ</i> genes recovered from soil is affiliated with <i>nosZ</i> found in the genomes of the obligate aerobic phylum <i>Gemmatimonadetes</i>, N₂O reduction has not yet been confirmed in any of these organisms. This study demonstrates that N₂O is reduced by an obligate aerobic bacterium, <i>Gemmatimonas aurantiaca</i> strain T-27, and suggests a novel regulation mechanism for N₂O reduction in this organism, which may also be applicable to other obligate aerobic organisms possessing <i>nosZ</i> genes. We expect that these findings will significantly advance the understanding of N₂O dynamics in environments with frequent transitions between oxic and anoxic conditions.