New insights into two yeast BDHs from the PDH subfamily as aldehyde reductases in context of detoxification of lignocellulosic aldehyde inhibitors

Kuang, Xiaolin; Ouyang, Yidan; Guo, Yaping; Li, Qian; Wang, Hanyu; Abrha, Getachew Tafere; Ayepa, Ellen; Gu, Yunfu; Li, Xi; Chen, Qiang; Ma, Menggen

doi:10.1007/s00253-020-10722-9

Applied genetics and molecular biotechnology
Published: 15 June 2020

New insights into two yeast BDHs from the PDH subfamily as aldehyde reductases in context of detoxification of lignocellulosic aldehyde inhibitors

Xiaolin Kuang¹^na1,
Yidan Ouyang¹^na1,
Yaping Guo^1,2,
Qian Li¹,
Hanyu Wang¹,
Getachew Tafere Abrha¹,
Ellen Ayepa¹,
Yunfu Gu³,
Xi Li⁴,
Qiang Chen³ &
Menggen Ma ORCID: orcid.org/0000-0002-1855-7064^1,3

Applied Microbiology and Biotechnology volume 104, pages 6679–6692 (2020)Cite this article

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Abstract

At least 24 aldehyde reductases from Saccharomyces cerevisiae have been characterized and most function in in situ detoxification of lignocellulosic aldehyde inhibitors, but none is classified into the polyol dehydrogenase (PDH) subfamily of the medium-chain dehydrogenase/reductase (MDR) superfamily. This study confirmed that two (2R,3R)-2,3-butanediol dehydrogenases (BDHs) from industrial (denoted Y)/laboratory (denoted B) strains of S. cerevisiae, Bdh1p(Y)/Bdh1p(B) and Bdh2p(Y)/Bdh2p(B), were members of the PDH subfamily with an NAD(P)H binding domain and a catalytic zinc binding domain, and exhibited reductive activities towards lignocellulosic aldehyde inhibitors, such as acetaldehyde, glycolaldehyde, and furfural. Especially, the highest enzyme activity towards acetaldehyde by Bdh2p(Y) was 117.95 U/mg with cofactor nicotinamide adenine dinucleotide reduced (NADH). Based on the comparative kinetic property analysis, Bdh2p(Y)/Bdh2p(B) possessed higher specific activity, substrate affinity, and catalytic efficiency towards glycolaldehyde than Bdh1p(Y)/Bdh1p(B). This was speculated to be related to their 49% sequence differences and five nonsynonymous substitutions (Ser41Thr, Glu173Gln, Ile270Leu, Ile316Met, and Gly317Cys) occurred in their conserved NAD(P)H binding domains. Compared with BDHs from a laboratory strain, Bdh1p(Y) and Bdh2p(Y) from an industrial strain displayed five nonsynonymous mutations (Thr¹², Asn⁶¹, Glu¹⁶⁸, Val²²², and Ala²³⁵) and three nonsynonymous mutations (Ala³⁴, Ile⁹⁶, and Ala³⁶⁹), respectively. From a first analysis with selected aldehydes, their reductase activities were different from BDHs of laboratory strain, and their catalytic efficiency was higher towards glycolaldehyde and lower towards acetaldehyde. Comparative investigation of kinetic properties of BDHs from S. cerevisiae as aldehyde reductases provides a guideline for their practical applications in in situ detoxification of aldehyde inhibitors during lignocellulose bioconversion.

Key Points

• Two yeast BDHs have enzyme activities for reduction of aldehydes.

• Overexpression of BDHs slightly improves yeast tolerance to acetaldehyde and glycolaldehyde.

• Bdh1p and Bdh2p differ in enzyme kinetic properties.

• BDHs from strains with different genetic backgrounds differ in enzyme kinetic properties.

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Acknowledgments

The authors thank James Allen from Liwen Bianji, Edanz Group China for revising this manuscript.

Funding

This work was funded by the Science and Technology Department of Sichuan Province (No. 2020YFH0142), the National Natural Science Foundation of China (No. 31570086), and the Talent Introduction Fund of Sichuan Agricultural University (No. 01426100).

Author information

Xiaolin Kuang and Yidan Ouyang contributed equally to this work.

Authors and Affiliations

Institute of Resources and Geographic Information Technology, College of Resources, Sichuan Agricultural University, No. 211 Huimin Road, Wenjiang, Chengdu, 611130, Sichuan, People’s Republic of China
Xiaolin Kuang, Yidan Ouyang, Yaping Guo, Qian Li, Hanyu Wang, Getachew Tafere Abrha, Ellen Ayepa & Menggen Ma
Patent Examination Cooperation Sichuan Center of the Patent Office, SIPO, Chengdu, 610213, Sichuan, People’s Republic of China
Yaping Guo
Department of Applied Microbiology, College of Resources, Sichuan Agricultural University, Wenjiang, Chengdu, 611130, Sichuan, People’s Republic of China
Yunfu Gu, Qiang Chen & Menggen Ma
College of Landscape Architecture, Sichuan Agricultural University, Wenjiang, Chengdu, 611130, Sichuan, People’s Republic of China
Xi Li

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Xiaolin Kuang
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Yidan Ouyang
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Yaping Guo
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Qian Li
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Hanyu Wang
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Getachew Tafere Abrha
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Ellen Ayepa
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Yunfu Gu
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Xi Li
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Qiang Chen
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Menggen Ma
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Contributions

MGM, XLK, and YDOY conceived and designed research. XLK, YDOY, YPG, QL, and HYW conducted experiments. XLK, YDOY, and YPG analyzed data. YFG, XL, and QC contributed analytical tools. XLK and YDOY wrote the manuscript. MGM, GTA, and EA revised the manuscript. All authors read and approved the manuscript.

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Correspondence to Menggen Ma.

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Kuang, X., Ouyang, Y., Guo, Y. et al. New insights into two yeast BDHs from the PDH subfamily as aldehyde reductases in context of detoxification of lignocellulosic aldehyde inhibitors. Appl Microbiol Biotechnol 104, 6679–6692 (2020). https://doi.org/10.1007/s00253-020-10722-9

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Received: 16 January 2020
Revised: 25 May 2020
Accepted: 04 June 2020
Published: 15 June 2020
Issue Date: August 2020
DOI: https://doi.org/10.1007/s00253-020-10722-9

Keywords

Aldehyde reductases
BDHs
Kinetic property
Lignocellulosic inhibitors
PDH (polyol dehydrogenase) subfamily