Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism

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 (acety...

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Autores principales:	Morgan N. Price, Jayashree Ray, Anthony T. Iavarone, Hans K. Carlson, Elizabeth M. Ryan, Rex R. Malmstrom, Adam P. Arkin, Adam M. Deutschbauer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	deoxyribonate catabolism deoxyribose catabolism high-throughput genetics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8c6070a8b917459bb98b8aa3d5d84032
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spelling	oai:doaj.org-article:8c6070a8b917459bb98b8aa3d5d840322021-12-02T19:47:33ZOxidative Pathways of Deoxyribose and Deoxyribonate Catabolism10.1128/mSystems.00297-182379-5077https://doaj.org/article/8c6070a8b917459bb98b8aa3d5d840322019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00297-18https://doaj.org/toc/2379-5077ABSTRACT 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.Morgan N. PriceJayashree RayAnthony T. IavaroneHans K. CarlsonElizabeth M. RyanRex R. MalmstromAdam P. ArkinAdam M. DeutschbauerAmerican Society for Microbiologyarticledeoxyribonate catabolismdeoxyribose catabolismhigh-throughput geneticsMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	deoxyribonate catabolism deoxyribose catabolism high-throughput genetics Microbiology QR1-502
spellingShingle	deoxyribonate catabolism deoxyribose catabolism high-throughput genetics Microbiology QR1-502 Morgan N. Price Jayashree Ray Anthony T. Iavarone Hans K. Carlson Elizabeth M. Ryan Rex R. Malmstrom Adam P. Arkin Adam M. Deutschbauer Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism
description	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.
format	article
author	Morgan N. Price Jayashree Ray Anthony T. Iavarone Hans K. Carlson Elizabeth M. Ryan Rex R. Malmstrom Adam P. Arkin Adam M. Deutschbauer
author_facet	Morgan N. Price Jayashree Ray Anthony T. Iavarone Hans K. Carlson Elizabeth M. Ryan Rex R. Malmstrom Adam P. Arkin Adam M. Deutschbauer
author_sort	Morgan N. Price
title	Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism
title_short	Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism
title_full	Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism
title_fullStr	Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism
title_full_unstemmed	Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism
title_sort	oxidative pathways of deoxyribose and deoxyribonate catabolism
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/8c6070a8b917459bb98b8aa3d5d84032
work_keys_str_mv	AT morgannprice oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism AT jayashreeray oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism AT anthonytiavarone oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism AT hanskcarlson oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism AT elizabethmryan oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism AT rexrmalmstrom oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism AT adamparkin oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism AT adammdeutschbauer oxidativepathwaysofdeoxyriboseanddeoxyribonatecatabolism
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Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism

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