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

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...

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Autores principales: Yoon, Sojung, Heo, Hokwan, Han, Heejoo, Song, Dong-Uk, Bakken, Lars R., Frostegård, Åsa, Yoon, Sukhwan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10653820/
https://www.ncbi.nlm.nih.gov/pubmed/37737639
http://dx.doi.org/10.1128/mbio.01540-23
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author Yoon, Sojung
Heo, Hokwan
Han, Heejoo
Song, Dong-Uk
Bakken, Lars R.
Frostegård, Åsa
Yoon, Sukhwan
author_facet Yoon, Sojung
Heo, Hokwan
Han, Heejoo
Song, Dong-Uk
Bakken, Lars R.
Frostegård, Åsa
Yoon, Sukhwan
author_sort Yoon, Sojung
collection PubMed
description 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.
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spelling pubmed-106538202023-09-22 Suggested role of NosZ in preventing N(2)O inhibition of dissimilatory nitrite reduction to ammonium Yoon, Sojung Heo, Hokwan Han, Heejoo Song, Dong-Uk Bakken, Lars R. Frostegård, Åsa Yoon, Sukhwan mBio Research Article 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. American Society for Microbiology 2023-09-22 /pmc/articles/PMC10653820/ /pubmed/37737639 http://dx.doi.org/10.1128/mbio.01540-23 Text en Copyright © 2023 Yoon et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Yoon, Sojung
Heo, Hokwan
Han, Heejoo
Song, Dong-Uk
Bakken, Lars R.
Frostegård, Åsa
Yoon, Sukhwan
Suggested role of NosZ in preventing N(2)O inhibition of dissimilatory nitrite reduction to ammonium
title Suggested role of NosZ in preventing N(2)O inhibition of dissimilatory nitrite reduction to ammonium
title_full Suggested role of NosZ in preventing N(2)O inhibition of dissimilatory nitrite reduction to ammonium
title_fullStr Suggested role of NosZ in preventing N(2)O inhibition of dissimilatory nitrite reduction to ammonium
title_full_unstemmed Suggested role of NosZ in preventing N(2)O inhibition of dissimilatory nitrite reduction to ammonium
title_short Suggested role of NosZ in preventing N(2)O inhibition of dissimilatory nitrite reduction to ammonium
title_sort suggested role of nosz in preventing n(2)o inhibition of dissimilatory nitrite reduction to ammonium
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10653820/
https://www.ncbi.nlm.nih.gov/pubmed/37737639
http://dx.doi.org/10.1128/mbio.01540-23
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