Suggested role of NosZ in preventing N 2 O inhibition of dissimilatory nitrite reduction to ammonium

Abstract

ABSTRACT Climate change and nutrient pollution are among the most urgent environmental issues. Enhancing the abundance and/or the activity of beneficial organisms is an attractive strategy to counteract these problems. Dissimilatory nitrate reduction to ammonium (DNRA), which theoretically improves nitrogen retention in soils, has been suggested as a microbial process that may be harnessed, especially since many DNRA-catalyzing organisms have been found to possess nosZ genes and the ability to respire N 2 O. However, the selective advantage that may favor these nosZ -harboring DNRA-catalyzing organisms is not well understood. Here, the effect of N 2 O on Nrf-mediated DNRA was examined in a soil isolate, Bacillus sp. DNRA2, possessing both nrfA and nosZ genes. The DNRA metabolism of this bacterium was observed in the presence of C 2 H 2, a NosZ inhibitor, with or without N 2 O, and the results were compared with C 2 H 2 -free controls. Cultures were also exposed to repeated oxic-anoxic transitions in the sustained presence of N 2 O. The NO 2 − -to-NH 4 + reduction following oxic-to-anoxic transition was significantly delayed in NosZ-inhibited C 2 H 2 -amended cultures, and the inhibition was more pronounced with repeated oxic-anoxic transitions. The possibility of C 2 H 2 involvement was dismissed since the cultures continuously flushed with C 2 H 2 /N 2 mixed gas after initial oxic incubation did not exhibit a similar delay in DNRA progression as that observed in the culture flushed with N 2 O-containing gas. The findings suggest a possibility that the oft-observed nosZ presence in DNRA-catalyzing microorganisms secures an early transcription of their DNRA genes by scavenging N 2 O, thus enhancing their capacity to compete with denitrifiers at oxic-anoxic interfaces. IMPORTANCE Dissimilatory nitrate/nitrite reduction to ammonium (DNRA) is a microbial energy-conserving process that reduces NO 3 − and/or NO 2 − to NH 4 + . Interestingly, DNRA-catalyzing microorganisms possessing nrfA genes are occasionally found harboring nosZ genes encoding nitrous oxide reductases, i.e., the only group of enzymes capable of removing the potent greenhouse gas N 2 O. Here, through a series of physiological experiments examining DNRA metabolism in one of such microorganisms, Bacillus sp. DNRA2, we have discovered that N 2 O may delay the transition to DNRA upon an oxic-to-anoxic transition, unless timely removed by the nitrous oxide reductases. These observations suggest a novel explanation as to why some nrfA -possessing microorganisms have retained nosZ genes: to remove N 2 O that may otherwise interfere with the transition from O 2 respiration to DNRA.