2,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolism

Abstract Overflow metabolism-caused acetate accumulation is a major problem that restricts industrial applications of various bacteria. 2,3-Butanediol (2,3-BD) synthesis in microorganisms is an ancient metabolic process with unidentified functions. We demonstrate here that acetate increases and then...

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Main Authors: Wensi Meng, Lijie Zhang, Menghao Cao, Yongjia Zhang, Yipeng Zhang, Ping Li, Zhaoqi Kang, Shiting Guo, Ping Xu, Cuiqing Ma, Chao Gao
Format: Article
Language:English
Published: Nature Publishing Group 2021-06-01
Series:Cell Discovery
Online Access:https://doi.org/10.1038/s41421-021-00273-2
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spelling doaj-d9d18904b4ea49aab08d5971979dbd202021-06-13T11:28:07ZengNature Publishing GroupCell Discovery2056-59682021-06-017111210.1038/s41421-021-00273-22,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolismWensi Meng0Lijie Zhang1Menghao Cao2Yongjia Zhang3Yipeng Zhang4Ping Li5Zhaoqi Kang6Shiting Guo7Ping Xu8Cuiqing Ma9Chao Gao10State Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, and School of Life Sciences & Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityState Key Laboratory of Microbial Technology, Shandong UniversityAbstract Overflow metabolism-caused acetate accumulation is a major problem that restricts industrial applications of various bacteria. 2,3-Butanediol (2,3-BD) synthesis in microorganisms is an ancient metabolic process with unidentified functions. We demonstrate here that acetate increases and then decreases during the growth of a bacterium Enterobacter cloacae subsp. dissolvens SDM. Both bifunctional acetaldehyde/ethanol dehydrogenase AdhE-catalyzed ethanol production and acetate-induced 2,3-BD biosynthesis are indispensable for the elimination of acetate generated during overflow metabolism. 2,3-BD biosynthesis from glucose supplies NADH required for acetate elimination via AdhE-catalyzed ethanol production. The coupling strategy involving 2,3-BD biosynthesis and ethanol production is widely distributed in bacteria and is important for toxic acetate elimination. Finally, we realized the co-production of ethanol and acetoin from chitin, the second most abundant natural biopolymer whose catabolism involves inevitable acetate production through the coupling acetate elimination strategy. The synthesis of a non-toxic chemical such as 2,3-BD may be viewed as a unique overflow metabolism with desirable metabolic functions.https://doi.org/10.1038/s41421-021-00273-2
collection DOAJ
language English
format Article
sources DOAJ
author Wensi Meng
Lijie Zhang
Menghao Cao
Yongjia Zhang
Yipeng Zhang
Ping Li
Zhaoqi Kang
Shiting Guo
Ping Xu
Cuiqing Ma
Chao Gao
spellingShingle Wensi Meng
Lijie Zhang
Menghao Cao
Yongjia Zhang
Yipeng Zhang
Ping Li
Zhaoqi Kang
Shiting Guo
Ping Xu
Cuiqing Ma
Chao Gao
2,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolism
Cell Discovery
author_facet Wensi Meng
Lijie Zhang
Menghao Cao
Yongjia Zhang
Yipeng Zhang
Ping Li
Zhaoqi Kang
Shiting Guo
Ping Xu
Cuiqing Ma
Chao Gao
author_sort Wensi Meng
title 2,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolism
title_short 2,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolism
title_full 2,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolism
title_fullStr 2,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolism
title_full_unstemmed 2,3-Butanediol synthesis from glucose supplies NADH for elimination of toxic acetate produced during overflow metabolism
title_sort 2,3-butanediol synthesis from glucose supplies nadh for elimination of toxic acetate produced during overflow metabolism
publisher Nature Publishing Group
series Cell Discovery
issn 2056-5968
publishDate 2021-06-01
description Abstract Overflow metabolism-caused acetate accumulation is a major problem that restricts industrial applications of various bacteria. 2,3-Butanediol (2,3-BD) synthesis in microorganisms is an ancient metabolic process with unidentified functions. We demonstrate here that acetate increases and then decreases during the growth of a bacterium Enterobacter cloacae subsp. dissolvens SDM. Both bifunctional acetaldehyde/ethanol dehydrogenase AdhE-catalyzed ethanol production and acetate-induced 2,3-BD biosynthesis are indispensable for the elimination of acetate generated during overflow metabolism. 2,3-BD biosynthesis from glucose supplies NADH required for acetate elimination via AdhE-catalyzed ethanol production. The coupling strategy involving 2,3-BD biosynthesis and ethanol production is widely distributed in bacteria and is important for toxic acetate elimination. Finally, we realized the co-production of ethanol and acetoin from chitin, the second most abundant natural biopolymer whose catabolism involves inevitable acetate production through the coupling acetate elimination strategy. The synthesis of a non-toxic chemical such as 2,3-BD may be viewed as a unique overflow metabolism with desirable metabolic functions.
url https://doi.org/10.1038/s41421-021-00273-2
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