A pathway for biological methane production using bacterial iron-only nitrogenase

Yanning Zheng; Derek F. Harris; Zheng Yu; Yanfen Fu; Saroj Poudel; Rhesa N. Ledbetter; Kathryn R. Fixen; Zhi Yong Yang; Eric S. Boyd; Mary E. Lidstrom; Lance C. Seefeldt; Caroline S. Harwood

doi:10.1038/s41564-017-0091-5

A pathway for biological methane production using bacterial iron-only nitrogenase

Yanning Zheng, Derek F. Harris, Zheng Yu, Yanfen Fu, Saroj Poudel, Rhesa N. Ledbetter, Kathryn R. Fixen, Zhi Yong Yang, Eric S. Boyd, Mary E. Lidstrom, Lance C. Seefeldt, Caroline S. Harwood

Plant and Microbial Biology

Research output: Contribution to journal › Article › peer-review

117 Scopus citations

Abstract

Methane (CH ₄ ) is a potent greenhouse gas that is released from fossil fuels and is also produced by microbial activity, with at least one billion tonnes of CH ₄ being formed and consumed by microorganisms in a single year ¹ . Complex methanogenesis pathways used by archaea are the main route for bioconversion of carbon dioxide (CO ₂ ) to CH ₄ in nature ^2-4 . Here, we report that wild-type iron-iron (Fe-only) nitrogenase from the bacterium Rhodopseudomonas palustris reduces CO ₂ simultaneously with nitrogen gas (N ₂ ) and protons to yield CH ₄ , ammonia (NH ₃ ) and hydrogen gas (H ₂ ) in a single enzymatic step. The amount of CH ₄ produced by purified Fe-only nitrogenase was low compared to its other products, but CH ₄ production by this enzyme in R. palustris was sufficient to support the growth of an obligate CH ₄ -utilizing Methylomonas strain when the two microorganisms were grown in co-culture, with oxygen (O ₂ ) added at intervals. Other nitrogen-fixing bacteria that we tested also formed CH ₄ when expressing Fe-only nitrogenase, suggesting that this is a general property of this enzyme. The genomes of 9% of diverse nitrogen-fixing microorganisms from a range of environments encode Fe-only nitrogenase. Our data suggest that active Fe-only nitrogenase, present in diverse microorganisms, contributes CH ₄ that could shape microbial community interactions.

Original language	English (US)
Pages (from-to)	281-286
Number of pages	6
Journal	Nature Microbiology
Volume	3
Issue number	3
DOIs	https://doi.org/10.1038/s41564-017-0091-5
State	Published - Mar 1 2018

Bibliographical note

Funding Information:
We thank the entire Biological Electron Transfer and Catalysis (BETCy) team for informative discussions. We also thank G. Roberts, Y. Zhang, J. McKinlay and F. Daldal for the generous gifts of R. rubrum and R. capsulatus strains, S. Shaw for assistance with activity assays and M. Tokmina-Lukaszewska for the verification of purified Fe-only nitrogenase by mass spectrometry. This work was supported as part of the BETCy Energy Frontier Research Center (EFRC), an EFRC funded by the US Department of Energy, Office of Science Grant DE-SC0012518.

Publisher Copyright:
© 2017 The Author(s).

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title = "A pathway for biological methane production using bacterial iron-only nitrogenase",

abstract = " Methane (CH 4 ) is a potent greenhouse gas that is released from fossil fuels and is also produced by microbial activity, with at least one billion tonnes of CH 4 being formed and consumed by microorganisms in a single year 1 . Complex methanogenesis pathways used by archaea are the main route for bioconversion of carbon dioxide (CO 2 ) to CH 4 in nature 2-4 . Here, we report that wild-type iron-iron (Fe-only) nitrogenase from the bacterium Rhodopseudomonas palustris reduces CO 2 simultaneously with nitrogen gas (N 2 ) and protons to yield CH 4 , ammonia (NH 3 ) and hydrogen gas (H 2 ) in a single enzymatic step. The amount of CH 4 produced by purified Fe-only nitrogenase was low compared to its other products, but CH 4 production by this enzyme in R. palustris was sufficient to support the growth of an obligate CH 4 -utilizing Methylomonas strain when the two microorganisms were grown in co-culture, with oxygen (O 2 ) added at intervals. Other nitrogen-fixing bacteria that we tested also formed CH 4 when expressing Fe-only nitrogenase, suggesting that this is a general property of this enzyme. The genomes of 9% of diverse nitrogen-fixing microorganisms from a range of environments encode Fe-only nitrogenase. Our data suggest that active Fe-only nitrogenase, present in diverse microorganisms, contributes CH 4 that could shape microbial community interactions.",

author = "Yanning Zheng and Harris, {Derek F.} and Zheng Yu and Yanfen Fu and Saroj Poudel and Ledbetter, {Rhesa N.} and Fixen, {Kathryn R.} and Yang, {Zhi Yong} and Boyd, {Eric S.} and Lidstrom, {Mary E.} and Seefeldt, {Lance C.} and Harwood, {Caroline S.}",

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AU - Seefeldt, Lance C.

AU - Harwood, Caroline S.

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A pathway for biological methane production using bacterial iron-only nitrogenase

Abstract

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