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

Author

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  • Mengxiong Wu

    (The University of Queensland)

  • Jie Li

    (The University of Queensland)

  • Andy O. Leu

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Dirk V. Erler

    (Southern Cross University)

  • Terra Stark

    (The University of Queensland)

  • Gene W. Tyson

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Zhiguo Yuan

    (The University of Queensland)

  • Simon J. McIlroy

    (Queensland University of Technology (QUT), Translational Research Institute)

  • Jianhua Guo

    (The University of Queensland)

Abstract

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 13C- and 15N-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 CO2 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.

Suggested Citation

  • Mengxiong Wu & Jie Li & Andy O. Leu & Dirk V. Erler & Terra Stark & Gene W. Tyson & Zhiguo Yuan & Simon J. McIlroy & Jianhua Guo, 2022. "Anaerobic oxidation of propane coupled to nitrate reduction by a lineage within the class Symbiobacteriia," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33872-y
    DOI: 10.1038/s41467-022-33872-y
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    References listed on IDEAS

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    1. Gunter Wegener & Viola Krukenberg & Dietmar Riedel & Halina E. Tegetmeyer & Antje Boetius, 2015. "Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria," Nature, Nature, vol. 526(7574), pages 587-590, October.
    2. Katharina F. Ettwig & Margaret K. Butler & Denis Le Paslier & Eric Pelletier & Sophie Mangenot & Marcel M. M. Kuypers & Frank Schreiber & Bas E. Dutilh & Johannes Zedelius & Dirk de Beer & Jolein Gloe, 2010. "Nitrite-driven anaerobic methane oxidation by oxygenic bacteria," Nature, Nature, vol. 464(7288), pages 543-548, March.
    3. Mohamed F. Haroon & Shihu Hu & Ying Shi & Michael Imelfort & Jurg Keller & Philip Hugenholtz & Zhiguo Yuan & Gene W. Tyson, 2013. "Erratum: Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage," Nature, Nature, vol. 501(7468), pages 578-578, September.
    4. Antje Boetius & Katrin Ravenschlag & Carsten J. Schubert & Dirk Rickert & Friedrich Widdel & Armin Gieseke & Rudolf Amann & Bo Barker Jørgensen & Ursula Witte & Olaf Pfannkuche, 2000. "A marine microbial consortium apparently mediating anaerobic oxidation of methane," Nature, Nature, vol. 407(6804), pages 623-626, October.
    5. Mohamed F. Haroon & Shihu Hu & Ying Shi & Michael Imelfort & Jurg Keller & Philip Hugenholtz & Zhiguo Yuan & Gene W. Tyson, 2013. "Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage," Nature, Nature, vol. 500(7464), pages 567-570, August.
    6. Song-Can Chen & Niculina Musat & Oliver J. Lechtenfeld & Heidrun Paschke & Matthias Schmidt & Nedal Said & Denny Popp & Federica Calabrese & Hryhoriy Stryhanyuk & Ulrike Jaekel & Yong-Guan Zhu & Saman, 2019. "Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep," Nature, Nature, vol. 568(7750), pages 108-111, April.
    7. Olaf Kniemeyer & Florin Musat & Stefan M. Sievert & Katrin Knittel & Heinz Wilkes & Martin Blumenberg & Walter Michaelis & Arno Classen & Carsten Bolm & Samantha B. Joye & Friedrich Widdel, 2007. "Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria," Nature, Nature, vol. 449(7164), pages 898-901, October.
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