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Title: Elucidation of roles for vitamin B 12 in regulation of folate, ubiquinone, and methionine metabolism

Abstract

Only a small fraction of vitamin B 12-requiring organisms are able to synthesize B 12 de novo, making it a common commodity in microbial communities. Initially recognized as an enzyme cofactor of a few enzymes, recent studies have revealed additional B 12-binding enzymes and regulatory roles for B 12. Here we report the development and use of a B 12-based chemical probe to identify B 12-binding proteins in a nonphototrophic B 12-producing bacterium. Two unexpected discoveries resulted from this study. First, we identified a new light-sensing B 12-binding transcriptional regulator and demonstrated that it controls folate and ubiquinone biosynthesis. Second, our probe captured proteins involved in folate, methionine, and ubiquinone metabolism suggesting that it may play a role as an allosteric effector of these processes. These metabolic processes produce precursors for synthesis of DNA, RNA, and protein. Furthermore, B 12 modulates growth, and by limiting its availability to auxotrophs, B 12-producing organisms may facilitate coordination of community metabolism.

Authors:
 [1];  [2];  [1];  [1];  [1];  [3];  [4];  [5];  [1];  [1]; ORCiD logo [1];  [1];  [1]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Russian Academy of Sciences, Moscow (Russia); Sanford-Burnham-Prebys Medical Discovery Institute, La Jolla, CA (United States)
  3. Sanford-Burnham-Prebys Medical Discovery Institute, La Jolla, CA (United States); Univ. of California, San Diego, La Jolla, CA (United States)
  4. Polytech Nice-Sophia, Biot (France)
  5. Sanford-Burnham-Prebys Medical Discovery Institute, La Jolla, CA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1341767
Alternate Identifier(s):
OSTI ID: 1347852
Report Number(s):
PNNL-SA-119181
Journal ID: ISSN 0027-8424; KP1601010
Grant/Contract Number:  
AC05-76RL01830; 58612
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 7; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; chemical biology; cobalamin; metabolism; microbial regulation

Citation Formats

Romine, Margaret F., Rodionov, Dmitry A., Maezato, Yukari, Anderson, Lindsey N., Nandhikonda, Premchendar, Rodionova, Irina A., Carre, Alexandre, Li, Xiaoqing, Xu, Chengdong, Clauss, Therese R. W., Kim, Young -Mo, Metz, Thomas O., and Wright, Aaron T.. Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism. United States: N. p., 2017. Web. doi:10.1073/pnas.1612360114.
Romine, Margaret F., Rodionov, Dmitry A., Maezato, Yukari, Anderson, Lindsey N., Nandhikonda, Premchendar, Rodionova, Irina A., Carre, Alexandre, Li, Xiaoqing, Xu, Chengdong, Clauss, Therese R. W., Kim, Young -Mo, Metz, Thomas O., & Wright, Aaron T.. Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism. United States. doi:10.1073/pnas.1612360114.
Romine, Margaret F., Rodionov, Dmitry A., Maezato, Yukari, Anderson, Lindsey N., Nandhikonda, Premchendar, Rodionova, Irina A., Carre, Alexandre, Li, Xiaoqing, Xu, Chengdong, Clauss, Therese R. W., Kim, Young -Mo, Metz, Thomas O., and Wright, Aaron T.. Mon . "Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism". United States. doi:10.1073/pnas.1612360114.
@article{osti_1341767,
title = {Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism},
author = {Romine, Margaret F. and Rodionov, Dmitry A. and Maezato, Yukari and Anderson, Lindsey N. and Nandhikonda, Premchendar and Rodionova, Irina A. and Carre, Alexandre and Li, Xiaoqing and Xu, Chengdong and Clauss, Therese R. W. and Kim, Young -Mo and Metz, Thomas O. and Wright, Aaron T.},
abstractNote = {Only a small fraction of vitamin B12-requiring organisms are able to synthesize B12 de novo, making it a common commodity in microbial communities. Initially recognized as an enzyme cofactor of a few enzymes, recent studies have revealed additional B12-binding enzymes and regulatory roles for B12. Here we report the development and use of a B12-based chemical probe to identify B12-binding proteins in a nonphototrophic B12-producing bacterium. Two unexpected discoveries resulted from this study. First, we identified a new light-sensing B12-binding transcriptional regulator and demonstrated that it controls folate and ubiquinone biosynthesis. Second, our probe captured proteins involved in folate, methionine, and ubiquinone metabolism suggesting that it may play a role as an allosteric effector of these processes. These metabolic processes produce precursors for synthesis of DNA, RNA, and protein. Furthermore, B12 modulates growth, and by limiting its availability to auxotrophs, B12-producing organisms may facilitate coordination of community metabolism.},
doi = {10.1073/pnas.1612360114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 7,
volume = 114,
place = {United States},
year = {Mon Jan 30 00:00:00 EST 2017},
month = {Mon Jan 30 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1073/pnas.1612360114

Citation Metrics:
Cited by: 3 works
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Works referenced in this record:

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