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Title: Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism

Abstract

ABSTRACT Using genome-wide mutant fitness assays in diverse bacteria, we identified novel oxidative pathways for the catabolism of 2-deoxy- d -ribose and 2-deoxy- d -ribonate. We propose that deoxyribose is oxidized to deoxyribonate, oxidized to ketodeoxyribonate, and cleaved to acetyl coenzyme A (acetyl-CoA) and glyceryl-CoA. We have genetic evidence for this pathway in three genera of bacteria, and we confirmed the oxidation of deoxyribose to ketodeoxyribonate in vitro . In Pseudomonas simiae , the expression of enzymes in the pathway is induced by deoxyribose or deoxyribonate, while in Paraburkholderia bryophila and in Burkholderia phytofirmans , the pathway proceeds in parallel with the known deoxyribose 5-phosphate aldolase pathway. We identified another oxidative pathway for the catabolism of deoxyribonate, with acyl-CoA intermediates, in Klebsiella michiganensis . Of these four bacteria, only P. simiae relies entirely on an oxidative pathway to consume deoxyribose. The deoxyribose dehydrogenase of P. simiae is either nonspecific or evolved recently, as this enzyme is very similar to a novel vanillin dehydrogenase from Pseudomonas putida that we identified. So, we propose that these oxidative pathways evolved primarily to consume deoxyribonate, which is a waste product of metabolism. IMPORTANCE Deoxyribose is one of the building blocks of DNA and ismore » released when cells die and their DNA degrades. We identified a bacterium that can grow with deoxyribose as its sole source of carbon even though its genome does not contain any of the known genes for breaking down deoxyribose. By growing many mutants of this bacterium together on deoxyribose and using DNA sequencing to measure the change in the mutants’ abundance, we identified multiple protein-coding genes that are required for growth on deoxyribose. Based on the similarity of these proteins to enzymes of known function, we propose a 6-step pathway in which deoxyribose is oxidized and then cleaved. Diverse bacteria use a portion of this pathway to break down a related compound, deoxyribonate, which is a waste product of metabolism. Our study illustrates the utility of large-scale bacterial genetics to identify previously unknown metabolic pathways.« less

Authors:
ORCiD logo [1];  [1];  [2];  [1];  [3];  [3];  [4];  [4];  [5]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  5. Ghent Univ. (Belgium)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1493373
Alternate Identifier(s):
OSTI ID: 1508059
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Published Article
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 4; Journal Issue: 1; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; deoxyribonate catabolism; deoxyribose catabolism; high-throughput genetics

Citation Formats

Price, Morgan N., Ray, Jayashree, Iavarone, Anthony T., Carlson, Hans K., Ryan, Elizabeth M., Malmstrom, Rex R., Arkin, Adam P., Deutschbauer, Adam M., and Rabaey, Korneel. Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism. United States: N. p., 2019. Web. doi:10.1128/msystems.00297-18.
Price, Morgan N., Ray, Jayashree, Iavarone, Anthony T., Carlson, Hans K., Ryan, Elizabeth M., Malmstrom, Rex R., Arkin, Adam P., Deutschbauer, Adam M., & Rabaey, Korneel. Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism. United States. doi:10.1128/msystems.00297-18.
Price, Morgan N., Ray, Jayashree, Iavarone, Anthony T., Carlson, Hans K., Ryan, Elizabeth M., Malmstrom, Rex R., Arkin, Adam P., Deutschbauer, Adam M., and Rabaey, Korneel. Tue . "Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism". United States. doi:10.1128/msystems.00297-18.
@article{osti_1493373,
title = {Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism},
author = {Price, Morgan N. and Ray, Jayashree and Iavarone, Anthony T. and Carlson, Hans K. and Ryan, Elizabeth M. and Malmstrom, Rex R. and Arkin, Adam P. and Deutschbauer, Adam M. and Rabaey, Korneel},
abstractNote = {ABSTRACT Using genome-wide mutant fitness assays in diverse bacteria, we identified novel oxidative pathways for the catabolism of 2-deoxy- d -ribose and 2-deoxy- d -ribonate. We propose that deoxyribose is oxidized to deoxyribonate, oxidized to ketodeoxyribonate, and cleaved to acetyl coenzyme A (acetyl-CoA) and glyceryl-CoA. We have genetic evidence for this pathway in three genera of bacteria, and we confirmed the oxidation of deoxyribose to ketodeoxyribonate in vitro . In Pseudomonas simiae , the expression of enzymes in the pathway is induced by deoxyribose or deoxyribonate, while in Paraburkholderia bryophila and in Burkholderia phytofirmans , the pathway proceeds in parallel with the known deoxyribose 5-phosphate aldolase pathway. We identified another oxidative pathway for the catabolism of deoxyribonate, with acyl-CoA intermediates, in Klebsiella michiganensis . Of these four bacteria, only P. simiae relies entirely on an oxidative pathway to consume deoxyribose. The deoxyribose dehydrogenase of P. simiae is either nonspecific or evolved recently, as this enzyme is very similar to a novel vanillin dehydrogenase from Pseudomonas putida that we identified. So, we propose that these oxidative pathways evolved primarily to consume deoxyribonate, which is a waste product of metabolism. IMPORTANCE Deoxyribose is one of the building blocks of DNA and is released when cells die and their DNA degrades. We identified a bacterium that can grow with deoxyribose as its sole source of carbon even though its genome does not contain any of the known genes for breaking down deoxyribose. By growing many mutants of this bacterium together on deoxyribose and using DNA sequencing to measure the change in the mutants’ abundance, we identified multiple protein-coding genes that are required for growth on deoxyribose. Based on the similarity of these proteins to enzymes of known function, we propose a 6-step pathway in which deoxyribose is oxidized and then cleaved. Diverse bacteria use a portion of this pathway to break down a related compound, deoxyribonate, which is a waste product of metabolism. Our study illustrates the utility of large-scale bacterial genetics to identify previously unknown metabolic pathways.},
doi = {10.1128/msystems.00297-18},
journal = {mSystems},
issn = {2379-5077},
number = 1,
volume = 4,
place = {United States},
year = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1128/msystems.00297-18

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Works referenced in this record:

MicrobesOnline: an integrated portal for comparative and functional genomics
journal, November 2009

  • Dehal, P. S.; Joachimiak, M. P.; Price, M. N.
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Rapid Quantification of Mutant Fitness in Diverse Bacteria by Sequencing Randomly Bar-Coded Transposons
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