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Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia

Anaerobic microorganisms are thought to play a critical role in regulating the flux of short-chain gaseous alkanes (SCGAs; including ethane, propane and butane) from terrestrial and aquatic ecosystems to the atmosphere. Sulfate has been confirmed to act as electron acceptor supporting microbial anae...

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Autores principales: Wu, Mengxiong, Li, Jie, Leu, Andy O., Erler, Dirk V., Stark, Terra, Tyson, Gene W., Yuan, Zhiguo, McIlroy, Simon J., Guo, Jianhua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9576796/
https://www.ncbi.nlm.nih.gov/pubmed/36253480
http://dx.doi.org/10.1038/s41467-022-33872-y
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author Wu, Mengxiong
Li, Jie
Leu, Andy O.
Erler, Dirk V.
Stark, Terra
Tyson, Gene W.
Yuan, Zhiguo
McIlroy, Simon J.
Guo, Jianhua
author_facet Wu, Mengxiong
Li, Jie
Leu, Andy O.
Erler, Dirk V.
Stark, Terra
Tyson, Gene W.
Yuan, Zhiguo
McIlroy, Simon J.
Guo, Jianhua
author_sort Wu, Mengxiong
collection PubMed
description Anaerobic microorganisms are thought to play a critical role in regulating the flux of short-chain gaseous alkanes (SCGAs; including ethane, propane and butane) from terrestrial and aquatic ecosystems to the atmosphere. Sulfate has been confirmed to act as electron acceptor supporting microbial anaerobic oxidation of SCGAs, yet several other energetically more favourable acceptors co-exist with these gases in anaerobic environments. Here, we show that a bioreactor seeded with biomass from a wastewater treatment facility can perform anaerobic propane oxidation coupled to nitrate reduction to dinitrogen gas and ammonium. The bioreactor was operated for more than 1000 days, and we used (13)C- and (15)N-labelling experiments, metagenomic, metatranscriptomic, metaproteomic and metabolite analyses to characterize the microbial community and the metabolic processes. The data collectively suggest that a species representing a novel order within the bacterial class Symbiobacteriia is responsible for the observed nitrate-dependent propane oxidation. The closed genome of this organism, which we designate as ‘Candidatus Alkanivorans nitratireducens’, encodes pathways for oxidation of propane to CO(2) via fumarate addition, and for nitrate reduction, with all the key genes expressed during nitrate-dependent propane oxidation. Our results suggest that nitrate is a relevant electron sink for SCGA oxidation in anaerobic environments, constituting a new microbially-mediated link between the carbon and nitrogen cycles.
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spelling pubmed-95767962022-10-19 Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia Wu, Mengxiong Li, Jie Leu, Andy O. Erler, Dirk V. Stark, Terra Tyson, Gene W. Yuan, Zhiguo McIlroy, Simon J. Guo, Jianhua Nat Commun Article Anaerobic microorganisms are thought to play a critical role in regulating the flux of short-chain gaseous alkanes (SCGAs; including ethane, propane and butane) from terrestrial and aquatic ecosystems to the atmosphere. Sulfate has been confirmed to act as electron acceptor supporting microbial anaerobic oxidation of SCGAs, yet several other energetically more favourable acceptors co-exist with these gases in anaerobic environments. Here, we show that a bioreactor seeded with biomass from a wastewater treatment facility can perform anaerobic propane oxidation coupled to nitrate reduction to dinitrogen gas and ammonium. The bioreactor was operated for more than 1000 days, and we used (13)C- and (15)N-labelling experiments, metagenomic, metatranscriptomic, metaproteomic and metabolite analyses to characterize the microbial community and the metabolic processes. The data collectively suggest that a species representing a novel order within the bacterial class Symbiobacteriia is responsible for the observed nitrate-dependent propane oxidation. The closed genome of this organism, which we designate as ‘Candidatus Alkanivorans nitratireducens’, encodes pathways for oxidation of propane to CO(2) via fumarate addition, and for nitrate reduction, with all the key genes expressed during nitrate-dependent propane oxidation. Our results suggest that nitrate is a relevant electron sink for SCGA oxidation in anaerobic environments, constituting a new microbially-mediated link between the carbon and nitrogen cycles. Nature Publishing Group UK 2022-10-17 /pmc/articles/PMC9576796/ /pubmed/36253480 http://dx.doi.org/10.1038/s41467-022-33872-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Wu, Mengxiong
Li, Jie
Leu, Andy O.
Erler, Dirk V.
Stark, Terra
Tyson, Gene W.
Yuan, Zhiguo
McIlroy, Simon J.
Guo, Jianhua
Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia
title Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia
title_full Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia
title_fullStr Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia
title_full_unstemmed Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia
title_short Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia
title_sort anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class symbiobacteriia
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9576796/
https://www.ncbi.nlm.nih.gov/pubmed/36253480
http://dx.doi.org/10.1038/s41467-022-33872-y
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