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Research Article

Acetogenic bacteria utilize light-driven electrons as an energy source for autotrophic growth

View ORCID ProfileSangrak Jin, Yale Jeon, Min Soo Jeon, Jongoh Shin, Yoseb Song, Seulgi Kang, Jiyun Bae, Suhyung Cho, View ORCID ProfileJung-Kul Lee, View ORCID ProfileDong Rip Kim, and Byung-Kwan Cho
  1. aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
  2. bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
  3. cDepartment of Mechanical Engineering, Hanyang University, 04763 Seoul, Republic of Korea;
  4. dDepartment of Chemical Engineering, Konkuk University, 05029 Seoul, Republic of Korea;
  5. eIntelligent Synthetic Biology Center, 34141 Daejeon, Republic of Korea

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PNAS March 2, 2021 118 (9) e2020552118; https://doi.org/10.1073/pnas.2020552118
Sangrak Jin
aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
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  • ORCID record for Sangrak Jin
Yale Jeon
cDepartment of Mechanical Engineering, Hanyang University, 04763 Seoul, Republic of Korea;
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Min Soo Jeon
cDepartment of Mechanical Engineering, Hanyang University, 04763 Seoul, Republic of Korea;
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Jongoh Shin
aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
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Yoseb Song
aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
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Seulgi Kang
aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
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Jiyun Bae
aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
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Suhyung Cho
aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
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Jung-Kul Lee
dDepartment of Chemical Engineering, Konkuk University, 05029 Seoul, Republic of Korea;
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Dong Rip Kim
cDepartment of Mechanical Engineering, Hanyang University, 04763 Seoul, Republic of Korea;
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Byung-Kwan Cho
aDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
bInnovative Biomaterials Research Center, KI for the BioCentury, Korea Advanced Institute of Science and Technology, 34141 Daejeon, Republic of Korea;
eIntelligent Synthetic Biology Center, 34141 Daejeon, Republic of Korea
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  • For correspondence: bcho@kaist.ac.kr
  1. Edited by Caroline S. Harwood, University of Washington, Seattle, WA, and approved January 20, 2021 (received for review October 1, 2020)

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Significance

To develop an efficient artificial photosynthesis system using acetogen-nanoparticle hybrids, the efficiency of the electron–hole pair generation of nanoparticles must be enhanced to demonstrate extracellular electron utilization by the acetogen. Here we verified that Clostridium autoethanogenum, an industrially relevant acetogen, could use electrons generated from size- and structure-controlled chemically synthesized cadmium sulfide nanoparticles displayed on the cell surface under light-exposure conditions. In addition, transcriptomic analysis showed that the electrons generated from nanoparticles were largely transported to the intracellular matrix via the metal ion or flavin-binding proteins. These results illustrate the potential to increase the CO2-fixing efficiency of nanoparticle-based artificial photosynthesis by engineering cellular processes related to electron transfer generated from the cathode.

Abstract

Acetogenic bacteria use cellular redox energy to convert CO2 to acetate using the Wood–Ljungdahl (WL) pathway. Such redox energy can be derived from electrons generated from H2 as well as from inorganic materials, such as photoresponsive semiconductors. We have developed a nanoparticle-microbe hybrid system in which chemically synthesized cadmium sulfide nanoparticles (CdS-NPs) are displayed on the cell surface of the industrial acetogen Clostridium autoethanogenum. The hybrid system converts CO2 into acetate without the need for additional energy sources, such as H2, and uses only light-induced electrons from CdS-NPs. To elucidate the underlying mechanism by which C. autoethanogenum uses electrons generated from external energy sources to reduce CO2, we performed transcriptional analysis. Our results indicate that genes encoding the metal ion or flavin-binding proteins were highly up-regulated under CdS-driven autotrophic conditions along with the activation of genes associated with the WL pathway and energy conservation system. Furthermore, the addition of these cofactors increased the CO2 fixation rate under light-exposure conditions. Our results demonstrate the potential to improve the efficiency of artificial photosynthesis systems based on acetogenic bacteria integrated with photoresponsive nanoparticles.

  • acetogenic bacteria
  • artificial photosynthesis
  • cadmium sulfide nanoparticle
  • extracellular electron transfer
  • Clostridium autoethanogenum

Footnotes

  • ↵1To whom correspondence may be addressed. Email: bcho{at}kaist.ac.kr.
  • Author contributions: B.-K.C. designed research; S.J., Y.J., M.S.J., J.S., Y.S., S.K., J.B., and S.C. performed research; S.J., S.C., J.-K.L., D.R.K., and B.-K.C. analyzed data; and S.J., S.C., and B.-K.C. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2020552118/-/DCSupplemental.

Data Availability

The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, https://www.ncbi.nlm.nih.gov/geo (accession no. GSE157613).

  • Copyright © 2021 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Acetogenic bacteria utilize light-driven electrons as an energy source for autotrophic growth
Sangrak Jin, Yale Jeon, Min Soo Jeon, Jongoh Shin, Yoseb Song, Seulgi Kang, Jiyun Bae, Suhyung Cho, Jung-Kul Lee, Dong Rip Kim, Byung-Kwan Cho
Proceedings of the National Academy of Sciences Mar 2021, 118 (9) e2020552118; DOI: 10.1073/pnas.2020552118

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Acetogenic bacteria utilize light-driven electrons as an energy source for autotrophic growth
Sangrak Jin, Yale Jeon, Min Soo Jeon, Jongoh Shin, Yoseb Song, Seulgi Kang, Jiyun Bae, Suhyung Cho, Jung-Kul Lee, Dong Rip Kim, Byung-Kwan Cho
Proceedings of the National Academy of Sciences Mar 2021, 118 (9) e2020552118; DOI: 10.1073/pnas.2020552118
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Proceedings of the National Academy of Sciences: 118 (9)
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