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PreprintCited by 11Microbial Fuel Cells and BioremediationMetalloenzymes and iron-sulfur proteinsMicrobial metabolism and enzyme function

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Electrochemical cofactor recycling of bacterial microcompartments

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Sutter, Markus, Utschig, Lisa M., Niklas, Jens, Paul, Sathi, Kahan, Darren N., Gupta, Sayan, Poluektov, Oleg G., Ferlez, Bryan H., Tefft, Nicholas M., TerAvest, Michaela A., Hickey, David P., Vermaas, Josh V., Ralston, Corie Y., Kerfeld, Cheryl A.·2024·Proceedings of the National Academy of Sciences
DOI 10.1101/2024.07.15.603600PMC PMC11626177

Preprint — published as 10.1073/pnas.2414220121

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Abstract

Bacterial microcompartments (BMCs) are prokaryotic organelles that consist of a protein shell which sequesters metabolic reactions in its interior. While most of the substrates and products are relatively small and can permeate the shell, many of the encapsulated enzymes require cofactors that must be regenerated inside. We have analyzed the occurrence of an enzyme previously assigned as a cobalamin (vitamin B 12 ) reductase and, curiously, found it in many unrelated BMC types that do not employ B 12 cofactors. We propose NAD+ regeneration as a new function of this enzyme and name it MNdh, for Metabolosome NADH dehydrogenase. Its partner shell protein BMC-T SE assists in passing the generated electrons to the outside. We support this hypothesis with bioinformatic analysis, functional assays, EPR spectroscopy, protein voltammetry and structural modeling verified with X-ray footprinting. This discovery represents a new paradigm for the BMC field, identifying a new, widely occurring route for cofactor recycling and a new function for the shell as separating redox environments.

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Metadata

Authors
Sutter, M., Utschig, L. M., Niklas, J., Paul, S., Kahan, D. N., Gupta, S., Poluektov, O. G., Ferlez, B. H., Tefft, N. M., TerAvest, M. A., Hickey, D. P., Vermaas, J. V., Ralston, C. Y., & Kerfeld, C. A.
Affiliations
  • Lawrence Berkeley National Laboratory (US)
  • Argonne National Laboratory (US)
  • University of California, Berkeley (US)
  • Michigan State University (US)
Corresponding author
  • Ferlez, Bryan H.
  • Kerfeld, Cheryl A.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
openRxiv
Published
2024-07-15
Volume
121
Issue
49
Pages
e2414220121-e2414220121
ISSN
0027-8424 (ISSN-L)
DOI
10.1101/2024.07.15.603600
PMC
PMC11626177
OpenAlex
W4404674479
Cited by
11
References
1
Citations by year
2026: 5 · 2025: 3 · 2024: 3
FWCI
1.28
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nd)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
Funders
  • U.S. Department of Energy (DE‐ AC02‐06CH11357, -AC02-05CH11231, DE‐FG02‐, DEFG0291ER20021, AC02‐06CH11357, 05CH11231, DE AC02 05CH11231, DE-SC0023395, 06CH11357, GM124169, FG0291ER20021, DE-AC02-)
  • National Institutes of Health (DE-AC02–05CH11231, DE-AC02–06CH11357, GM124169)
  • Office of Science (AC02‐06CH11357, DEAC02–05CH11231, AC02-05CH11231, DE-AC02, 06CH11357, DEFG0291ER20021, DE-AC02-06CH11357)
  • National Institute of General Medical Sciences (P30GM124169, R01GM126218)
  • Basic Energy Sciences (DE- FG02-91ER20021, DE-AC02, DE-AC02-05CH11231., DE-AC- 02-06CH11357, AC02‐06CH11357, DE-FG02, AC02–05CH11231, 06CH11357, DE‐SC0023395, FG02-91ER20021)
  • Argonne National Laboratory (DE- AC02-06-CH11357, DE-AC02, AC02–06CH11357, DE-AC02-05CH11231, 06CH11357)
  • Lawrence Berkeley National Laboratory (AC02‐05CH11231, DE-AC02-05CH11231, DE-AC02-06CH11357, 05CH11231)
Topics
  • Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
Keywords
bacterial microcompartments, cofactor recycling, NAD+ regeneration, NADH dehydrogenase, electron transfer

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