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Title: Alternative pathways utilize or circumvent putrescine for biosynthesis of putrescine-containing rhizoferrin

Abstract

The siderophore rhizoferrin (N1,N4-dicitrylputrescine) is produced in fungi and bacteria to scavenge iron. Putrescine-producing bacterium Ralstonia pickettii synthesizes rhizoferrin and encodes a single nonribosomal peptide synthetase-independent siderophore (NIS) synthetase. From biosynthetic logic, we hypothesized that this single enzyme is sufficient for rhizoferrin biosynthesis. We confirmed this by expression of R. pickettii NIS synthetase in Escherichia coli, resulting in rhizoferrin production. This was further confirmed in vitro using the recombinant NIS synthetase, synthesizing rhizoferrin from putrescine and citrate. Heterologous expression of homologous lbtA from Legionella pneumophila, required for rhizoferrin biosynthesis in that species, produced siderophore activity in E. coli. Rhizoferrin is also synthesized by Francisella tularensis and Francisella novicida, but unlike R. pickettii or L. pneumophila, Francisella species lack putrescine biosynthetic pathways because of genomic decay. Francisella encodes a NIS synthetase FslA/FigA and an ornithine decarboxylase homolog FslC/FigC, required for rhizoferrin biosynthesis. Ornithine decarboxylase produces putrescine from ornithine, but we show here in vitro that FigA synthesizes N-citrylornithine, and FigC is an N-citrylornithine decarboxylase that together synthesize rhizoferrin without using putrescine. We co-expressed F. novicida figA and figC in E. coli and produced rhizoferrin. A 2.1 Å X-ray crystal structure of the FigC N-citrylornithine decarboxylase reveals how the larger substrate ismore » accommodated and how active site residues have changed to recognize N-citrylornithine. FigC belongs to a new subfamily of alanine racemase-fold PLP-dependent decarboxylases that are not involved in polyamine biosynthesis. These data reveal a natural product biosynthetic workaround that evolved to bypass a missing precursor and re-establish it in the final structure.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]
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  1. Univ. of Texas Southwestern Medical Center, Dallas, TX (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1765190
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 296; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Li, Bin, Deng, Xiaoyi, Kim, Sok Ho, Buhrow, Leann, Tomchick, Diana R., Phillips, Margaret A., and Michael, Anthony J. Alternative pathways utilize or circumvent putrescine for biosynthesis of putrescine-containing rhizoferrin. United States: N. p., 2021. Web. doi:10.1074/jbc.ra120.016738.
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Li, Bin, Deng, Xiaoyi, Kim, Sok Ho, Buhrow, Leann, Tomchick, Diana R., Phillips, Margaret A., & Michael, Anthony J. Alternative pathways utilize or circumvent putrescine for biosynthesis of putrescine-containing rhizoferrin. United States. https://doi.org/10.1074/jbc.ra120.016738
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Li, Bin, Deng, Xiaoyi, Kim, Sok Ho, Buhrow, Leann, Tomchick, Diana R., Phillips, Margaret A., and Michael, Anthony J. Fri . "Alternative pathways utilize or circumvent putrescine for biosynthesis of putrescine-containing rhizoferrin". United States. https://doi.org/10.1074/jbc.ra120.016738. https://www.osti.gov/servlets/purl/1765190.
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@article{osti_1765190,
title = {Alternative pathways utilize or circumvent putrescine for biosynthesis of putrescine-containing rhizoferrin},
author = {Li, Bin and Deng, Xiaoyi and Kim, Sok Ho and Buhrow, Leann and Tomchick, Diana R. and Phillips, Margaret A. and Michael, Anthony J.},
abstractNote = {The siderophore rhizoferrin (N1,N4-dicitrylputrescine) is produced in fungi and bacteria to scavenge iron. Putrescine-producing bacterium Ralstonia pickettii synthesizes rhizoferrin and encodes a single nonribosomal peptide synthetase-independent siderophore (NIS) synthetase. From biosynthetic logic, we hypothesized that this single enzyme is sufficient for rhizoferrin biosynthesis. We confirmed this by expression of R. pickettii NIS synthetase in Escherichia coli, resulting in rhizoferrin production. This was further confirmed in vitro using the recombinant NIS synthetase, synthesizing rhizoferrin from putrescine and citrate. Heterologous expression of homologous lbtA from Legionella pneumophila, required for rhizoferrin biosynthesis in that species, produced siderophore activity in E. coli. Rhizoferrin is also synthesized by Francisella tularensis and Francisella novicida, but unlike R. pickettii or L. pneumophila, Francisella species lack putrescine biosynthetic pathways because of genomic decay. Francisella encodes a NIS synthetase FslA/FigA and an ornithine decarboxylase homolog FslC/FigC, required for rhizoferrin biosynthesis. Ornithine decarboxylase produces putrescine from ornithine, but we show here in vitro that FigA synthesizes N-citrylornithine, and FigC is an N-citrylornithine decarboxylase that together synthesize rhizoferrin without using putrescine. We co-expressed F. novicida figA and figC in E. coli and produced rhizoferrin. A 2.1 Å X-ray crystal structure of the FigC N-citrylornithine decarboxylase reveals how the larger substrate is accommodated and how active site residues have changed to recognize N-citrylornithine. FigC belongs to a new subfamily of alanine racemase-fold PLP-dependent decarboxylases that are not involved in polyamine biosynthesis. These data reveal a natural product biosynthetic workaround that evolved to bypass a missing precursor and re-establish it in the final structure.},
doi = {10.1074/jbc.ra120.016738},
journal = {Journal of Biological Chemistry},
number = ,
volume = 296,
place = {United States},
year = {Fri Jan 01 00:00:00 EST 2021},
month = {Fri Jan 01 00:00:00 EST 2021}
}
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