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 ketodeoxyribonatein vitro. InPseudomonas simiae, the expression of enzymes in the pathway is induced by deoxyribose or deoxyribonate, while inParaburkholderia bryophilaand inBurkholderia 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, inKlebsiella michiganensis. Of these four bacteria, onlyP. simiaerelies entirely on an oxidative pathway to consume deoxyribose. The deoxyribose dehydrogenase ofP. simiaeis either nonspecific or evolved recently, as this enzyme is very similar to a novel vanillin dehydrogenase fromPseudomonas putidathat we identified. So, we propose that these oxidative pathways evolved primarily to consume deoxyribonate, which is a waste product of metabolism. IMPORTANCEDeoxyribose 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 sourcemore »
- Authors:
-
- Environmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, California, USA
- QB3/Chemistry Mass Spectrometry Facility, University of California, Berkeley, California, USA
- DOE Joint Genome Institute, Walnut Creek, California, USA
- Environmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, California, USA, Department of Bioengineering, University of California, Berkeley, California, USA
- Environmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, California, USA, Department of Plant and Microbial Biology, University of California, Berkeley, California, USA
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1493373
- Alternate Identifier(s):
- OSTI ID: 1508059
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Name: mSystems 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, ed., 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, ed., Korneel. Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism. United States. https://doi.org/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, ed., Korneel. Tue .
"Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism". United States. https://doi.org/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, ed., 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 ketodeoxyribonatein vitro. InPseudomonas simiae, the expression of enzymes in the pathway is induced by deoxyribose or deoxyribonate, while inParaburkholderia bryophilaand inBurkholderia 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, inKlebsiella michiganensis. Of these four bacteria, onlyP. simiaerelies entirely on an oxidative pathway to consume deoxyribose. The deoxyribose dehydrogenase ofP. simiaeis either nonspecific or evolved recently, as this enzyme is very similar to a novel vanillin dehydrogenase fromPseudomonas putidathat we identified. So, we propose that these oxidative pathways evolved primarily to consume deoxyribonate, which is a waste product of metabolism. IMPORTANCEDeoxyribose 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},
number = 1,
volume = 4,
place = {United States},
year = {2019},
month = {2}
}
https://doi.org/10.1128/mSystems.00297-18
Web of Science
Works referenced in this record:
The Primary Structure of Escherichia coli K12 2-Deoxyribose 5-Phosphate Aldolase : Nucleotide Sequence of the deoC Gene and the Amino Acid Sequence of the Enzyme
journal, July 1982
- Valentin-Hansen, Poul; BoËTius, Finn; Hammer-Jespersen, Karin
- European Journal of Biochemistry, Vol. 125, Issue 3
CDD: NCBI's conserved domain database
journal, November 2014
- Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R.
- Nucleic Acids Research, Vol. 43, Issue D1
MicrobesOnline: an integrated portal for comparative and functional genomics
journal, November 2009
- Dehal, P. S.; Joachimiak, M. P.; Price, M. N.
- Nucleic Acids Research, Vol. 38, Issue suppl_1, p. D396-D400
UPLC/MSE; a new approach for generating molecular fragment information for biomarker structure elucidation
journal, January 2006
- Plumb, Robert S.; Johnson, Kelly A.; Rainville, Paul
- Rapid Communications in Mass Spectrometry, Vol. 20, Issue 13
Mutant phenotypes for thousands of bacterial genes of unknown function
journal, May 2018
- Price, Morgan N.; Wetmore, Kelly M.; Waters, R. Jordan
- Nature, Vol. 557, Issue 7706
Cycling of extracellular DNA in the soil environment
journal, December 2007
- Levy-Booth, David J.; Campbell, Rachel G.; Gulden, Robert H.
- Soil Biology and Biochemistry, Vol. 39, Issue 12
‘Nothing of chemistry disappears in biology’: the Top 30 damage-prone endogenous metabolites
journal, June 2016
- Lerma-Ortiz, Claudia; Jeffryes, James G.; Cooper, Arthur J. L.
- Biochemical Society Transactions, Vol. 44, Issue 3
An Estimate of the Total DNA in the Biosphere
journal, June 2015
- Landenmark, Hanna K. E.; Forgan, Duncan H.; Cockell, Charles S.
- PLOS Biology, Vol. 13, Issue 6
Molecular Cloning of the Isoquinoline 1-Oxidoreductase Genes from Pseudomonas diminuta 7, Structural Analysis of IorA and IorB, and Sequence Comparisons with Other Molybdenum-containing Hydroxylases
journal, June 1995
- Lehmann, Martin; Tshisuaka, Barbara; Fetzner, Susanne
- Journal of Biological Chemistry, Vol. 270, Issue 24
CceR and AkgR Regulate Central Carbon and Energy Metabolism in Alphaproteobacteria
journal, February 2015
- Imam, Saheed; Noguera, Daniel R.; Donohue, Timothy J.
- mBio, Vol. 6, Issue 1
A metabolic pathway for catabolizing levulinic acid in bacteria
journal, September 2017
- Rand, Jacqueline M.; Pisithkul, Tippapha; Clark, Ryan L.
- Nature Microbiology, Vol. 2, Issue 12
Phosphate Starvation-Inducible Gene ushA Encodes a 5' Nucleotidase Required for Growth of Corynebacterium glutamicum on Media with Nucleotides as the Phosphorus Source
journal, August 2005
- Rittmann, D.; Sorger-Herrmann, U.; Wendisch, V. F.
- Applied and Environmental Microbiology, Vol. 71, Issue 8
Metabolic profiles of urinary organic acids recovered from absorbent filter paper.
journal, April 1987
- Chamberlin, B. A.; Sweeley, C. C.
- Clinical Chemistry, Vol. 33, Issue 4
Nucleosidases from Leishmania donovani. Pyrimidine ribonucleosidase, purine ribonucleosidase, and a novel purine 2'-deoxyribonucleosidase.
journal, October 1979
- Koszalka, G. W.; Krenitsky, T. A.
- Journal of Biological Chemistry, Vol. 254, Issue 17
Improvements to PATRIC, the all-bacterial Bioinformatics Database and Analysis Resource Center
journal, November 2016
- Wattam, Alice R.; Davis, James J.; Assaf, Rida
- Nucleic Acids Research, Vol. 45, Issue D1
TIGRFAMs and Genome Properties in 2013
journal, November 2012
- Haft, Daniel H.; Selengut, Jeremy D.; Richter, Roland A.
- Nucleic Acids Research, Vol. 41, Issue D1
Less label, more free: Approaches in label-free quantitative mass spectrometry
journal, January 2011
- Neilson, Karlie A.; Ali, Naveid A.; Muralidharan, Sridevi
- PROTEOMICS, Vol. 11, Issue 4
Microbial Metabolism of 2-Deoxyglucose; 2-Deoxygluconic Acid Dehydrogenase *
journal, January 1965
- Eichhorn, Mary M.; Cynkin, Morris A.
- Biochemistry, Vol. 4, Issue 1
Effects of Traveling Wave Ion Mobility Separation on Data Independent Acquisition in Proteomics Studies
journal, May 2013
- Shliaha, Pavel V.; Bond, Nicholas J.; Gatto, Laurent
- Journal of Proteome Research, Vol. 12, Issue 6
Metabolic Footprinting of Mutant Libraries to Map Metabolite Utilization to Genotype
journal, October 2012
- Baran, Richard; Bowen, Benjamin P.; Price, Morgan N.
- ACS Chemical Biology, Vol. 8, Issue 1
Comprehensive proteome analysis of the response of Pseudomonas putida KT2440 to the flavor compound vanillin
journal, September 2014
- Simon, Oliver; Klaiber, Iris; Huber, Armin
- Journal of Proteomics, Vol. 109
Rapid Quantification of Mutant Fitness in Diverse Bacteria by Sequencing Randomly Bar-Coded Transposons
journal, May 2015
- Wetmore, Kelly M.; Price, Morgan N.; Waters, Robert J.
- mBio, Vol. 6, Issue 3, Article No. e00306-15
Genome-wide identification of bacterial plant colonization genes
journal, September 2017
- Cole, Benjamin J.; Feltcher, Meghan E.; Waters, Robert J.
- PLOS Biology, Vol. 15, Issue 9
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013
- Overbeek, Ross; Olson, Robert; Pusch, Gordon D.
- Nucleic Acids Research, Vol. 42, Issue D1
Revealing the hidden functional diversity of an enzyme family
journal, November 2013
- Bastard, Karine; Smith, Adam Alexander Thil; Vergne-Vaxelaire, Carine
- Nature Chemical Biology, Vol. 10, Issue 1
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes
journal, May 2010
- Yu, Nancy Y.; Wagner, James R.; Laird, Matthew R.
- Bioinformatics, Vol. 26, Issue 13
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
The mutarotation of 2-deoxy-β-d-erythro-pentose (“2-deoxy-β-d-ribose”)
journal, November 1971
- Lemieux, R. U.; Anderson, Laurens; Conner, Anthony H.
- Carbohydrate Research, Vol. 20, Issue 1
Identification of 2-deoxyribonolactone at the site of neocarzinostatin-induced cytosine release in the sequence d(AGC)
journal, February 1989
- Kappen, Lizzy S.; Goldberg, Irving H.
- Biochemistry, Vol. 28, Issue 3
l-Arabinose/d-galactose 1-dehydrogenase of Rhizobium leguminosarum bv. trifolii characterised and applied for bioconversion of l-arabinose to l-arabonate with Saccharomyces cerevisiae
journal, September 2014
- Aro-Kärkkäinen, Niina; Toivari, Mervi; Maaheimo, Hannu
- Applied Microbiology and Biotechnology, Vol. 98, Issue 23
Only plant-type (GLYK) glycerate kinases produce d -glycerate 3-phosphate
journal, August 2008
- Bartsch, Oliver; Hagemann, Martin; Bauwe, Hermann
- FEBS Letters, Vol. 582, Issue 20
Genetic engineering of Pseudomonas putida KT2440 for rapid and high-yield production of vanillin from ferulic acid
journal, October 2013
- Graf, Nadja; Altenbuchner, Josef
- Applied Microbiology and Biotechnology, Vol. 98, Issue 1
RegPrecise 3.0 – A resource for genome-scale exploration of transcriptional regulation in bacteria
journal, January 2013
- Novichkov, Pavel S.; Kazakov, Alexey E.; Ravcheev, Dmitry A.
- BMC Genomics, Vol. 14, Issue 1
Identification and Characterization of l-Arabonate Dehydratase, l-2-Keto-3-deoxyarabonate Dehydratase, and l-Arabinolactonase Involved in an Alternative Pathway of l-Arabinose Metabolism: Novel Evolutionary Insight into Sugar Metabolism
journal, September 2006
- Watanabe, Seiya; Shimada, Naoko; Tajima, Kunihiko
- Journal of Biological Chemistry, Vol. 281, Issue 44, p. 33521-33536
An In Vivo Metabolic Approach for Deciphering the Product Specificity of Glycerate Kinase Proves that Both E. coli’s Glycerate Kinases Generate 2-Phosphoglycerate
journal, March 2015
- Zelcbuch, Lior; Razo-Mejia, Manuel; Herz, Elad
- PLOS ONE, Vol. 10, Issue 3
Drift time-specific collision energies enable deep-coverage data-independent acquisition proteomics
journal, December 2013
- Distler, Ute; Kuharev, Jörg; Navarro, Pedro
- Nature Methods, Vol. 11, Issue 2
Crystal structure and mechanism of CO dehydrogenase, a molybdo iron-sulfur flavoprotein containing S-selanylcysteine
journal, August 1999
- Dobbek, H.; Gremer, L.; Meyer, O.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 16
KEGG as a reference resource for gene and protein annotation
journal, October 2015
- Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki
- Nucleic Acids Research, Vol. 44, Issue D1