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Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris

Author

Listed:
  • Michael S. Guzman

    (Washington University in St. Louis)

  • Karthikeyan Rengasamy

    (Washington University in St. Louis)

  • Michael M. Binkley

    (Washington University in St. Louis)

  • Clive Jones

    (Washington University in St. Louis)

  • Tahina Onina Ranaivoarisoa

    (Washington University in St. Louis)

  • Rajesh Singh

    (Washington University in St. Louis)

  • David A. Fike

    (Washington University in St. Louis)

  • J. Mark Meacham

    (Washington University in St. Louis
    Washington University in St. Louis)

  • Arpita Bose

    (Washington University in St. Louis)

Abstract

Extracellular electron uptake (EEU) is the ability of microbes to take up electrons from solid-phase conductive substances such as metal oxides. EEU is performed by prevalent phototrophic bacterial genera, but the electron transfer pathways and the physiological electron sinks are poorly understood. Here we show that electrons enter the photosynthetic electron transport chain during EEU in the phototrophic bacterium Rhodopseudomonas palustris TIE-1. Cathodic electron flow is also correlated with a highly reducing intracellular redox environment. We show that reducing equivalents are used for carbon dioxide (CO2) fixation, which is the primary electron sink. Deletion of the genes encoding ruBisCO (the CO2-fixing enzyme of the Calvin-Benson-Bassham cycle) leads to a 90% reduction in EEU. This work shows that phototrophs can directly use solid-phase conductive substances for electron transfer, energy transduction, and CO2 fixation.

Suggested Citation

  • Michael S. Guzman & Karthikeyan Rengasamy & Michael M. Binkley & Clive Jones & Tahina Onina Ranaivoarisoa & Rajesh Singh & David A. Fike & J. Mark Meacham & Arpita Bose, 2019. "Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09377-6
    DOI: 10.1038/s41467-019-09377-6
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    Cited by:

    1. Na Chen & Na Du & Ruichen Shen & Tianpei He & Jing Xi & Jie Tan & Guangkai Bian & Yanbing Yang & Tiangang Liu & Weihong Tan & Lilei Yu & Quan Yuan, 2023. "Redox signaling-driven modulation of microbial biosynthesis and biocatalysis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Weiming Tu & Jiabao Xu & Ian P. Thompson & Wei E. Huang, 2023. "Engineering artificial photosynthesis based on rhodopsin for CO2 fixation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Guoping Ren & Jie Ye & Qichang Hu & Dong Zhang & Yong Yuan & Shungui Zhou, 2024. "Growth of electroautotrophic microorganisms using hydrovoltaic energy through natural water evaporation," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    4. Chen, Han & Huang, Yu & Sha, Chong & Moradian, Jamile Mohammadi & Yong, Yang-Chun & Fang, Zhen, 2023. "Enzymatic carbon dioxide to formate: Mechanisms, challenges and opportunities," Renewable and Sustainable Energy Reviews, Elsevier, vol. 178(C).
    5. Pan, Qin & Tian, Xiaochun & Li, Junpeng & Wu, Xuee & Zhao, Feng, 2021. "Interfacial electron transfer for carbon dioxide valorization in hybrid inorganic-microbial systems," Applied Energy, Elsevier, vol. 292(C).

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