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Title: A directed-overflow and damage-control N -glycosidase in riboflavin biosynthesis

Abstract

Plants and bacteria synthesize the essential human micronutrient riboflavin (vitamin B2) via the same multistep pathway. The early intermediates of this pathway are notoriously reactive, and may be overproduced in vivo because riboflavin biosynthesis enzymes lack feedback controls. Here we demonstrate disposal of riboflavin intermediates by COG3236 (DUF1768), a protein of previously unknown function that is fused to two different riboflavin pathway enzymes in plants and bacteria (RIBR and RibA, respectively). We present cheminformatic, biochemical, genetic, and genomic evidence to show that: (i) plant and bacterial COG3236 proteins cleave the N-glycosidic bond of the first two intermediates of riboflavin biosynthesis, yielding relatively innocuous products; (ii) certain COG3236 proteins are in a multienzyme riboflavin biosynthesis complex that gives them privileged access to riboflavin intermediates; and (iii) COG3236 action in Arabidopsis thaliana and Escherichia coli helps maintain flavin levels. We find COG3236 proteins thus illustrate two emerging principles in chemical biology: directed overflow metabolism, in which excess flux is diverted out of a pathway, and the pre-emption of damage from reactive metabolites.

Authors:
 [1];  [2];  [1];  [3];  [1];  [4];  [5];  [6];  [6];  [6];  [2];  [5];  [7];  [8];  [1]
+ Show Author Affiliations
  1. Univ. of Florida, Gainesville, FL (United States). Horticultural Sciences Dept.
  2. Univ. of Florida, Gainesville, FL (United States). Food Science and Human Nutrition Dept.
  3. Northwestern Univ., Evanston, IL (United States). Dept. of Chemical and Biological Engineering; Argonne National Lab. (ANL), Argonne, IL (United States). Mathematics and Computer Science Division
  4. Univ. of Florida, Gainesville, FL (United States). McKnight Brain Inst.
  5. Univ. of Florida, Gainesville, FL (United States). Dept. of Biochemistry and Molecular Biology
  6. Washington State Univ., Pullman, WA (United States). Inst. of Biological Chemistry
  7. Argonne National Lab. (ANL), Argonne, IL (United States). Mathematics and Computer Science Division; Univ. of Chicago, IL (United States). Computation Inst.
  8. Univ. of Florida, Gainesville, FL (United States). Dept. of Microbiology and Cell Science
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE; National Science Foundation (NSF)
OSTI Identifier:
1280875
Grant/Contract Number:  
IOS-1025398; 1U24DK097209-01A1; MCB-1153413; MCB-1153357
Resource Type:
Accepted Manuscript
Journal Name:
Biochemical Journal
Additional Journal Information:
Journal Volume: 466; Journal Issue: 1; Journal ID: ISSN 0264-6021
Publisher:
Biochemical Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Arabidopsis thaliana; Maillard cascade; metabolite damage; Vibrio vulnificus; vitamin B2; Zea mays

Citation Formats

Frelin, Océane, Huang, Lili, Hasnain, Ghulam, Jeffryes, James G., Ziemak, Michael J., Rocca, James R., Wang, Bing, Rice, Jennifer, Roje, Sanja, Yurgel, Svetlana N., Gregory, Jesse F., Edison, Arthur S., Henry, Christopher  S., de Crécy-Lagard, Valérie, and Hanson, Andrew D. A directed-overflow and damage-control N -glycosidase in riboflavin biosynthesis. United States: N. p., 2015. Web. doi:10.1042/bj20141237.
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Frelin, Océane, Huang, Lili, Hasnain, Ghulam, Jeffryes, James G., Ziemak, Michael J., Rocca, James R., Wang, Bing, Rice, Jennifer, Roje, Sanja, Yurgel, Svetlana N., Gregory, Jesse F., Edison, Arthur S., Henry, Christopher  S., de Crécy-Lagard, Valérie, & Hanson, Andrew D. A directed-overflow and damage-control N -glycosidase in riboflavin biosynthesis. United States. https://doi.org/10.1042/bj20141237
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Frelin, Océane, Huang, Lili, Hasnain, Ghulam, Jeffryes, James G., Ziemak, Michael J., Rocca, James R., Wang, Bing, Rice, Jennifer, Roje, Sanja, Yurgel, Svetlana N., Gregory, Jesse F., Edison, Arthur S., Henry, Christopher  S., de Crécy-Lagard, Valérie, and Hanson, Andrew D. Sun . "A directed-overflow and damage-control N -glycosidase in riboflavin biosynthesis". United States. https://doi.org/10.1042/bj20141237. https://www.osti.gov/servlets/purl/1280875.
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@article{osti_1280875,
title = {A directed-overflow and damage-control N -glycosidase in riboflavin biosynthesis},
author = {Frelin, Océane and Huang, Lili and Hasnain, Ghulam and Jeffryes, James G. and Ziemak, Michael J. and Rocca, James R. and Wang, Bing and Rice, Jennifer and Roje, Sanja and Yurgel, Svetlana N. and Gregory, Jesse F. and Edison, Arthur S. and Henry, Christopher  S. and de Crécy-Lagard, Valérie and Hanson, Andrew D.},
abstractNote = {Plants and bacteria synthesize the essential human micronutrient riboflavin (vitamin B2) via the same multistep pathway. The early intermediates of this pathway are notoriously reactive, and may be overproduced in vivo because riboflavin biosynthesis enzymes lack feedback controls. Here we demonstrate disposal of riboflavin intermediates by COG3236 (DUF1768), a protein of previously unknown function that is fused to two different riboflavin pathway enzymes in plants and bacteria (RIBR and RibA, respectively). We present cheminformatic, biochemical, genetic, and genomic evidence to show that: (i) plant and bacterial COG3236 proteins cleave the N-glycosidic bond of the first two intermediates of riboflavin biosynthesis, yielding relatively innocuous products; (ii) certain COG3236 proteins are in a multienzyme riboflavin biosynthesis complex that gives them privileged access to riboflavin intermediates; and (iii) COG3236 action in Arabidopsis thaliana and Escherichia coli helps maintain flavin levels. We find COG3236 proteins thus illustrate two emerging principles in chemical biology: directed overflow metabolism, in which excess flux is diverted out of a pathway, and the pre-emption of damage from reactive metabolites.},
doi = {10.1042/bj20141237},
journal = {Biochemical Journal},
number = 1,
volume = 466,
place = {United States},
year = {Sun Feb 15 00:00:00 EST 2015},
month = {Sun Feb 15 00:00:00 EST 2015}
}
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https://doi.org/10.1042/bj20141237
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Figures / Tables:

Figure 1 Figure 1: Evidence connecting COG3236 with riboflavin biosynthesis (A) The first three steps of riboflavin biosynthesis and their enzymes in bacteria (above arrows) and plants (below arrows). Steps two and three in bacteria are catalyzed by RibD, a bifunctional deamin-ase-reductase. RibA and RIBA1, GTP cyclohydrolase II; RibD and PYRD, pyrimidinemore » deaminase; RibD and RIBR, pyrimidine reductase. Intermediates 1, 2, and 3 are 2,5-diamino-6-ribosylamino-4(3H)-pyrimidinone 5′-phosphate, 5-amino-6ribosylamino-2,4(1H,3H)-pyrimidinedione 5′-phosphate, and 5-amino-6ribitylamino-2,4(1H,3H)-pyrimidinedione 5′-phosphate, respectively; P, phosphate. (B) Domain structures of fusions between COG3236 and RibA in γ-Proteobacteria, and between COG3236 and RIBR in plants. Two stand-alone bacterial COG3236 proteins are also shown. TP, plastid targeting peptide.« less
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