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Title: A bifunctional salvage pathway for two distinct S-adenosylmethionine byproducts that is widespread in bacteria, including pathogenic Escherichia coli

Abstract

S-adenosyl-L-methionine (SAM) is a necessary co-substrate for numerous essential enzymatic reactions including protein and nucleotide methylations, secondary metabolite synthesis, and radical-mediated processes. Radical SAM enzymes produce 5’-deoxyadenosine, and SAM-dependent enzymes for polyamine, neurotransmitter, and quorum sensing compound synthesis produce 5’-methylthioadenosine as byproducts. Both are inhibitory and must be addressed by all cells. This work establishes a bifunctional oxygen-independent salvage pathway for 5’-deoxyadenosine and 5’-methylthioadenosine in both Rhodospirillum rubrum and Extraintestinal Pathogenic Escherichia coli. Homologous genes for this pathway are widespread in bacteria, notably pathogenic strains within several families. A phosphorylase (Rhodospirillum rubrum) or separate nucleoside and kinase (Escherichia coli) followed by an isomerase and aldolase sequentially function to salvage these two wasteful and inhibitory compounds into adenine, dihydroxyacetone phosphate and acetaldehyde or (2-methylthio)acetaldehyde during both aerobic and anaerobic growth. Both SAM byproducts are metabolized with equal affinity during aerobic and anaerobic growth conditions, suggesting that the dual-purpose salvage pathway plays a central role in numerous environments, notably the human body during infection. Our newly discovered bifunctional oxygen-independent pathway, widespread in bacteria, salvages at least two byproducts of SAM-dependent enzymes for carbon and sulfur salvage, contributing to cell growth.

Authors:
 [1];  [1];  [2];  [3];  [1];  [4];  [1]
  1. Department of Microbiology The Ohio State University Columbus Ohio USA43120
  2. Max Planck Institute for Terrestrial Microbiology Department of Biochemistry and Synthetic Metabolism D‐35043Marburg Germany
  3. The Donald Danforth Plant Science Center St. Louis MO USA62132
  4. The Institute for Genomic Biology Department of Biochemistry Department of Chemistry University of Illinois at Urbana‐Champaign UrbanaUSA1206
Publication Date:
Research Org.:
The Ohio State Univ., Columbus, OH (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23). Biological Systems Science Division; USDOE
OSTI Identifier:
1593716
Alternate Identifier(s):
OSTI ID: 1601018
Grant/Contract Number:  
[SC0019338]
Resource Type:
Accepted Manuscript
Journal Name:
Molecular microbiology
Additional Journal Information:
[ Related Information: mmi14499-sup0001-Suppinfo]; Journal ID: ISSN 0950-382X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; 54 ENVIRONMENTAL SCIENCES; S-Adenosylmethionine, methionine, Dihydroxyacetone Phosphate, Bacteria, Rhodospirillum rubrum, Extraintestinal Pathogenic Escherichia coli

Citation Formats

North, Justin A., Wildenthal, John A., Erb, Tobias J., Evans, Bradley S., Byerly, Kathryn M., Gerlt, John A., and Tabita, F. Robert. A bifunctional salvage pathway for two distinct S-adenosylmethionine byproducts that is widespread in bacteria, including pathogenic Escherichia coli. United States: N. p., 2020. Web. doi:10.1111/MMI.14459.
North, Justin A., Wildenthal, John A., Erb, Tobias J., Evans, Bradley S., Byerly, Kathryn M., Gerlt, John A., & Tabita, F. Robert. A bifunctional salvage pathway for two distinct S-adenosylmethionine byproducts that is widespread in bacteria, including pathogenic Escherichia coli. United States. doi:10.1111/MMI.14459.
North, Justin A., Wildenthal, John A., Erb, Tobias J., Evans, Bradley S., Byerly, Kathryn M., Gerlt, John A., and Tabita, F. Robert. Fri . "A bifunctional salvage pathway for two distinct S-adenosylmethionine byproducts that is widespread in bacteria, including pathogenic Escherichia coli". United States. doi:10.1111/MMI.14459.
@article{osti_1593716,
title = {A bifunctional salvage pathway for two distinct S-adenosylmethionine byproducts that is widespread in bacteria, including pathogenic Escherichia coli},
author = {North, Justin A. and Wildenthal, John A. and Erb, Tobias J. and Evans, Bradley S. and Byerly, Kathryn M. and Gerlt, John A. and Tabita, F. Robert},
abstractNote = {S-adenosyl-L-methionine (SAM) is a necessary co-substrate for numerous essential enzymatic reactions including protein and nucleotide methylations, secondary metabolite synthesis, and radical-mediated processes. Radical SAM enzymes produce 5’-deoxyadenosine, and SAM-dependent enzymes for polyamine, neurotransmitter, and quorum sensing compound synthesis produce 5’-methylthioadenosine as byproducts. Both are inhibitory and must be addressed by all cells. This work establishes a bifunctional oxygen-independent salvage pathway for 5’-deoxyadenosine and 5’-methylthioadenosine in both Rhodospirillum rubrum and Extraintestinal Pathogenic Escherichia coli. Homologous genes for this pathway are widespread in bacteria, notably pathogenic strains within several families. A phosphorylase (Rhodospirillum rubrum) or separate nucleoside and kinase (Escherichia coli) followed by an isomerase and aldolase sequentially function to salvage these two wasteful and inhibitory compounds into adenine, dihydroxyacetone phosphate and acetaldehyde or (2-methylthio)acetaldehyde during both aerobic and anaerobic growth. Both SAM byproducts are metabolized with equal affinity during aerobic and anaerobic growth conditions, suggesting that the dual-purpose salvage pathway plays a central role in numerous environments, notably the human body during infection. Our newly discovered bifunctional oxygen-independent pathway, widespread in bacteria, salvages at least two byproducts of SAM-dependent enzymes for carbon and sulfur salvage, contributing to cell growth.},
doi = {10.1111/MMI.14459},
journal = {Molecular microbiology},
number = ,
volume = ,
place = {United States},
year = {2020},
month = {1}
}

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