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Title: Structural and Functional Characterization of a Short-Chain Flavodoxin Associated with a Noncanonical 1,2-Propanediol Utilization Bacterial Microcompartment

Abstract

Bacterial microcompartments (BMCs) are proteinaceous organelles that encapsulate enzymes involved in CO 2 fixation (carboxysomes). or carbon catabolism (metabolosomes). Metabolosomes share a common core of enzymes and a distinct signature enzyme for substrate degradation that defines the function of the BMC (e,g., propanediol or ethanolamine utilization BMCs, or glycyl-radical enzyme microcompartments). Loci encoding metabolosomes also typically contain genes for proteins that support organelle function, such as regulation, transport of substrate, and cofactor (e.g., vitamin B-12) synthesis and recycling. Flavoproteins are frequently among these ancillary gene products, suggesting that these redox active proteins play an undetermined function in many metabolosomes. Here in this paper, we report the first characterization of a BMC-associated flavodoxin (Fld1C), a small flavoprotein, derived from the noncanonical 1,2-propanediol utilization BMC locus (PDU1C) of Lactobacillus reuteri. The 2.0 angstrom X-ray structure of Fld1C displays the alpha/beta flavodoxin fold, which noncovalently binds a single flavin mononucleotide molecule. Fld1C is a short-chain flavodoxin with redox potentials of -240 +/- 3 mV oxidized/semiquinone and -344 +/- 1 mV semiquinone/hydroquinone versus the standard hydrogen electrode at pH 7.5. It can participate in an electron transfer reaction with a photoreductant to form a stable semiquinone species. Collectively, our structural and functional results suggestmore » that PDU1C BMCs encapsulate Fld1C to store and transfer electrons for the reactivation and/or recycling of the B 12 cofactor utilized by the signature enzyme.« less

Authors:
 [1];  [2];  [1];  [1]; ORCiD logo [3];  [3];  [1];  [4]; ORCiD logo [3];  [3]; ORCiD logo [5]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Solar Energy Conversion Group
  4. Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry & Molecular Biology
  5. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry & Molecular Biology; Berkeley Synthetic Biology Inst., Berkeley, CA (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1422561
Grant/Contract Number:  
[AC02-06CH11357]
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
[ Journal Volume: 56; Journal Issue: 42]; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Plegaria, Jefferson S., Sutter, Markus, Ferlez, Bryan, Aussignargues, Clement, Niklas, Jens, Poluektov, Oleg G., Fromwiller, Ciara, TerAvest, Michaela, Utschig, Lisa M., Tiede, David M., and Kerfeld, Cheryl A. Structural and Functional Characterization of a Short-Chain Flavodoxin Associated with a Noncanonical 1,2-Propanediol Utilization Bacterial Microcompartment. United States: N. p., 2017. Web. doi:10.1021/acs.biochem.7b00682.
Plegaria, Jefferson S., Sutter, Markus, Ferlez, Bryan, Aussignargues, Clement, Niklas, Jens, Poluektov, Oleg G., Fromwiller, Ciara, TerAvest, Michaela, Utschig, Lisa M., Tiede, David M., & Kerfeld, Cheryl A. Structural and Functional Characterization of a Short-Chain Flavodoxin Associated with a Noncanonical 1,2-Propanediol Utilization Bacterial Microcompartment. United States. doi:10.1021/acs.biochem.7b00682.
Plegaria, Jefferson S., Sutter, Markus, Ferlez, Bryan, Aussignargues, Clement, Niklas, Jens, Poluektov, Oleg G., Fromwiller, Ciara, TerAvest, Michaela, Utschig, Lisa M., Tiede, David M., and Kerfeld, Cheryl A. Thu . "Structural and Functional Characterization of a Short-Chain Flavodoxin Associated with a Noncanonical 1,2-Propanediol Utilization Bacterial Microcompartment". United States. doi:10.1021/acs.biochem.7b00682. https://www.osti.gov/servlets/purl/1422561.
@article{osti_1422561,
title = {Structural and Functional Characterization of a Short-Chain Flavodoxin Associated with a Noncanonical 1,2-Propanediol Utilization Bacterial Microcompartment},
author = {Plegaria, Jefferson S. and Sutter, Markus and Ferlez, Bryan and Aussignargues, Clement and Niklas, Jens and Poluektov, Oleg G. and Fromwiller, Ciara and TerAvest, Michaela and Utschig, Lisa M. and Tiede, David M. and Kerfeld, Cheryl A.},
abstractNote = {Bacterial microcompartments (BMCs) are proteinaceous organelles that encapsulate enzymes involved in CO2 fixation (carboxysomes). or carbon catabolism (metabolosomes). Metabolosomes share a common core of enzymes and a distinct signature enzyme for substrate degradation that defines the function of the BMC (e,g., propanediol or ethanolamine utilization BMCs, or glycyl-radical enzyme microcompartments). Loci encoding metabolosomes also typically contain genes for proteins that support organelle function, such as regulation, transport of substrate, and cofactor (e.g., vitamin B-12) synthesis and recycling. Flavoproteins are frequently among these ancillary gene products, suggesting that these redox active proteins play an undetermined function in many metabolosomes. Here in this paper, we report the first characterization of a BMC-associated flavodoxin (Fld1C), a small flavoprotein, derived from the noncanonical 1,2-propanediol utilization BMC locus (PDU1C) of Lactobacillus reuteri. The 2.0 angstrom X-ray structure of Fld1C displays the alpha/beta flavodoxin fold, which noncovalently binds a single flavin mononucleotide molecule. Fld1C is a short-chain flavodoxin with redox potentials of -240 +/- 3 mV oxidized/semiquinone and -344 +/- 1 mV semiquinone/hydroquinone versus the standard hydrogen electrode at pH 7.5. It can participate in an electron transfer reaction with a photoreductant to form a stable semiquinone species. Collectively, our structural and functional results suggest that PDU1C BMCs encapsulate Fld1C to store and transfer electrons for the reactivation and/or recycling of the B12 cofactor utilized by the signature enzyme.},
doi = {10.1021/acs.biochem.7b00682},
journal = {Biochemistry},
number = [42],
volume = [56],
place = {United States},
year = {2017},
month = {9}
}

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