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

Abstract

N 2 O-reducing organisms with nitrous oxide reductases (NosZ) are known as the only biological sink of N 2 O in the environment. Among the most abundant nosZ genes found in the environment are nosZ genes affiliated with the understudied Gemmatimonadetes phylum. In this study, a unique regulatory mechanism of N 2 O reduction in Gemmatimonas aurantiaca strain T-27, an isolate affiliated with the Gemmatimonadetes phylum, was examined. Strain T-27 was incubated with N 2 O and/or O 2 as the electron acceptor. Significant N 2 O reduction was observed only when O 2 was initially present. When batch cultures of strain T-27 were amended with O 2 and N 2 O, N 2 O reduction commenced after O 2 was depleted. In a long-term incubation with the addition of N 2 O upon depletion, the N 2 O reduction rate decreased over time and came to an eventual stop. Spiking of the culture with O 2 resulted in the resuscitation of N 2 O reduction activity, supporting the hypothesis that N 2 O reduction by strain T-27 required the transient presence of O 2 . The highest level of nosZ transcription (8.97 nosZ transcripts/recA transcript) was observed immediately after O 2 depletion, and transcription decreased ϳ25-fold within 85 h, supporting the observed phenotype. The observed difference between responses of strain T-27 cultures amended with and without N 2 O to O 2 starvation suggested that N 2 O helped sustain the viability of strain T-27 during temporary anoxia, although N 2 O reduction was not coupled to growth. The findings in this study suggest that obligate aerobic microorganisms with nosZ genes may utilize N 2 O as a temporary surrogate for O 2 to survive periodic anoxia.IMPORTANCE Emission of N 2 O, a potent greenhouse gas and ozone depletion agent, from the soil environment is largely determined by microbial sources and sinks. N 2 O reduction by organisms with N 2 O reductases (NosZ) is the only known biological sink of N 2 O at environmentally relevant concentrations (up to ϳ1,000 parts per million by volume [ppmv]). Although a large fraction of nosZ genes recovered from soil is affiliated with nosZ found in the genomes of the obligate aerobic phylum Gemmatimonadetes, N 2 O reduction has not yet been confirmed in any of these organisms. This study demonstrates that N 2 O is reduced by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27, and suggests a novel regulation mechanism for N 2 O reduction in this organism, which may also be applicable to other obligate aerobic organisms possessing nosZ genes. We expect that these findings will significantly advance the understanding of N 2 O dynamics in environments with frequent transitions between oxic and anoxic conditions.

Molecular Ecological Network Complexity Drives Stand Resilience of Soil Bacteria to Mining Disturbances among Typical Damaged Ecosystems in China

“…Recently, phylum Gemmatimonadetes has been described as a bacterial group whose members are widespread in soil habitats. Its cultured representative genus is Gemmatimonas aurantiaca, which has been isolated and is able to grow under not only anaerobic conditions but also aerobic conditions [44,45]. This finding might suggest that Gemmatimonadetes could be a suitable phylum in complicated mining areas that contain aerobic and anaerobic environmental habitats.…”

A widely distributed hydrogenase oxidises atmospheric H2during bacterial growth

“…For example, the metabolic generalist C. aggregans may facilitate its expansion in geothermal mats by simultaneously utilising geothermal and atmospheric sources of H 2 , in addition to sunlight and organic compounds [39, 40, 56]. Similarly, in the dynamic environment of wastewater treatment plants, G. aurantiaca may be well-suited to take advantage of fermentatively-produced H 2 released during transitions between oxic and anoxic states [36, 57].…”

“…To do so, we studied this enzyme in three species, Gemmatimonas aurantiaca , Acidithiobacillus ferrooxidans , and Chloroflexus aggregans , that differ in their phylogenetic affiliation, ecological niches, and metabolic strategies. The obligate chemoorganoheterotroph G. aurantiaca (phylum Gemmatimonadota) was originally isolated from a wastewater treatment plant and to date has not been shown to utilise H 2 [35, 36]. The obligate chemolithoautotroph A. ferrooxidans (phylum Proteobacteria) was originally isolated from acidic coal mine effluent, and has been extensively studied for its energetic flexibility, including the ability to grow exclusively on H 2 [32, 37, 38].…”

The influences of thorny bamboo growth on the bacterial community in badland soils of southwestern Taiwan

“…Analysis of Gemmatimonadetes 16S rRNA gene sequences from various ecosystems indicates that they are adapted to low soil moisture, which could explain their presence in this harsh badland ecosystem (DeBruyn et al, ). In addition, Park, Kim, and Yoon () revealed a unique regulatory mechanism of N 2 O reduction in an obligate aerobic Gemmatimonas strain, suggesting that this strain may play a role in nitrogen cycling in this ecosystem.…”