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YKL107W from Saccharomyces Cerevisiae Encodes a Novel Aldehyde Reductase for Detoxification of Acetaldehyde, Glycolaldehyde, and Furfural

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YKL107W from Saccharomyces Cerevisiae Encodes a Novel Aldehyde Reductase for Detoxification of Acetaldehyde, Glycolaldehyde, and Furfural YKL107W from Saccharomyces cerevisiae encodes a novel aldehyde reductase for detoxification of acetaldehyde, glycolaldehyde, and furfural Hanyu Wang, Qian Li, Zhengyue Zhang, Chang Zhou, Ellen Ayepa, Getachew Tafere Abrha, Xuebing Han, Xiangdong Hu, Xiumei Yu, et al. Applied Microbiology and Biotechnology ISSN 0175-7598 Volume 103 Number 14 Appl Microbiol Biotechnol (2019) 103:5699-5713 DOI 10.1007/s00253-019-09885-x 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag GmbH Germany, part of Springer Nature. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Applied Microbiology and Biotechnology (2019) 103:5699–5713 https://doi.org/10.1007/s00253-019-09885-x BIOTECHNOLOGICALLY RELEVANT ENZYMES AND PROTEINS YKL107W from Saccharomyces cerevisiae encodes a novel aldehyde reductase for detoxification of acetaldehyde, glycolaldehyde, and furfural Hanyu Wang1 & Qian Li1 & Zhengyue Zhang1 & Chang Zhou1 & Ellen Ayepa1 & Getachew Tafere Abrha1 & Xuebing Han1 & Xiangdong Hu1 & Xiumei Yu2 & Quanju Xiang2 & Xi Li3 & Yunfu Gu2 & Ke Zhao2 & Chengcheng Xie3 & Qiang Chen2 & Menggen Ma1,2 Received: 10 March 2019 /Revised: 24 April 2019 /Accepted: 29 April 2019 /Published online: 21 May 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract The aldehyde reductases from the short-chain dehydrogenase/reductase (SDR) family were identified as a series of critical enzymes for the improved tolerance of Saccharomyces cerevisiae to the aldehydes by catalyzing the detoxification reactions of aldehydes. Herein, we report that a novel aldehyde reductase Ykl107wp deduced from YKL107W from S. cerevisiae belongs to the classical SDR group and can catalyze the reduction reactions of acetaldehyde (AA), glycolaldehyde (GA), furfural (FF), formaldehyde (FA), and propionaldehyde (PA) but cannot reduce the six representative ketones. Ykl107wp displayed the best maximum velocity (Vmax), catalytic rate constant (Kcat), catalytic efficiency (Kcat/Km), and highest affinity (Km) to acetaldehyde. The optimum pH of Ykl107wp was 6.0 for the reduction of AA and 7.0 for the reduction of GA and FF, and the optimum temperatures were 40, 35, and 30 °C for the reduction of AA, GA, and FF, respectively. Ykl107wp for the reduction of AA was greatly affected by metal ions, chemical additives, and salts and showed poor thermal and pH stability, but its stability was slightly affected by a substrate. Ykl107wp was localized in endoplasmic reticulum and prevented the yeast cells from damage caused by furfural via the detoxification of furfural to furfural alcohol. This research provides guidelines for the study of uncharacterized classical SDR aldehyde reductases and exploration of their protective mechanisms on the corresponding organelles. Keywords Aldehyde reductase . Open reading frame . Protein-GFP localization·Saccharomyces cerevisiae . Short-chain dehydrogenase/reductase (SDR) Introduction Nicotinamide adenine dinucleotide (NADH)- and/or nicotin- Hanyu Wang, Qian Li and Zhengyue Zhang contributed equally to this work. amide adenine dinucleotide phosphate (NADPH)-dependent aldehyde reductases play critical roles for the improved toler- Electronic supplementary material The online version of this article ance of Saccharomyces cerevisiae to the aldehydes by in situ (https://doi.org/10.1007/s00253-019-09885-x) contains supplementary material, which is available to authorized users. detoxifying aldehydes to the less toxic corresponding alcohols (Gutiérrez et al. 2002;Liu2011; Liu et al. 2004). Recent studies * Menggen Ma found that aldehyde reductases not only catalyzed the reduction [email protected] of external aldehydes but also had abilities to degrade the en- dogenous aldehydes derived from the metabolism of amino 1 Institute of Resources and Geographic Information Technology, acids, carbohydrates, lipids, biogenic amines, vitamins, and ste- College of Resources, Sichuan Agricultural University, No. 211 Huimin Road, Wenjiang 611130, Sichuan, People’sRepublicof roids for sustaining the homeostasis of yeast cells (Hazelwood China et al. 2008; Vasiliou et al. 2000). To date, 24 aldehyde reduc- 2 Department of Applied Microbiology, College of Resources, Sichuan tases have been characterized in S. cerevisiae (Wang et al. Agricultural University, Wenjiang 611130, Sichuan, People’s 2018). Given the chain length, conserved functional motifs, Republic of China and structural features, these aldehyde reductases could be clas- 3 College of Landscape Architecture, Sichuan Agricultural University, sified into the medium-chain dehydrogenase/reductase (MDR) Wenjiang 611130, Sichuan, People’s Republic of China family, aldo-keto reductase (AKR) family, and short-chain Author's personal copy 5700 Appl Microbiol Biotechnol (2019) 103:5699–5713 dehydrogenase/reductase (SDR) family, but part of these reduc- Although Gre2p shows preference for NADH in the reduction tases, such as Adh4p, Ald4p, and Ald6p, could not be classified reactions of most of aldehydes, Gre2p has preference for (Kavanagh et al. 2008; Nordling et al. 2002; Persson et al. 1999, NADPH rather than NADH for the reduction of methylglyoxal 2008;Wangetal.2018). Protein sequence alignment analysis and isovaleraldehyde (Chen et al. 2003;Hauseretal.2007), found that most of the aldehyde reductases from the SDR fam- which is attributed to the hydrogen bonds between Asn9, ily are shorter than those from the MDR and AKR family in Arg32, and Lys36 and the phosphate moiety of adenosine (Guo length (Kavanagh et al. 2008). Significantly, Ykl071wp (256 et al. 2014). Additionally, substitutionofVal285byAspinGre2p amino acids, aa) as the classical SDR was identified as the can improve cofactor preference for NADPH than NADH in the shortest one among the 24 aldehyde reductases characterized reduction of FF and HMF (Moon and Liu 2012). However, the in S. cerevisiae (Wang et al. 2017a). The SDR aldehyde reduc- mechanisms of cofactor preference of other SDR aldehyde re- tases show similarity to the structure of the aldehyde reductases ductases were still unknown. Probably, the discoveries of novel in MDR family which contain cofactor-binding domain aldehyde reductases and the development of experiments on ami- (Rossmann fold) and substrate-binding sites (Kavanagh et al. no acid substitution will accelerate the elucidation of the molec- 2008; Persson et al. 2009;Wangetal.2018). Based on the ular mechanism of cofactor preference. Until now, the subcellular Rossmann fold, cofactor-binding domain, and C-terminal re- localization of the SDR aldehyde reductases was identified. gion, over 140,000 SDR members can be classified into 6 Ygl039wp, Yll056cp, and Ykl071wp were localized in the cyto- groups, namely Bclassical,^ Bextended,^ Bintermediate,^ plasm, Gre2p and Ari1p were localized in the cytoplasm/nucleus, Bdivergent,^ Bcomplex,^ and Batypical^ groups (Jornvall while Ydr541cp was localized in endoplasmic reticulum (ER) et al. 2015; Marchler-Bauer et al. 2013, 2015). Until now, the (Huh et al. 2003;Wangetal.2017b;Yofeetal.2016). Since six characterized SDR aldehyde reductases (Ari1p, Ygl039wp, exogenous aldehydes can pass through subcellular membranes Gre2p, Ydr541cp, Ykl071wp, and Yll056cp) were included in (such as mitochondrial membrane, vacuole membrane, and nu- the Bintermediate,^ Bclassical,^ and Batypical^ subfamilies in clear membrane) and enter the organelles and induce damages of the SDR family (Wang et al. 2018). Even though these alde- organelles (Allen et al. 2010; Voulgaridou et al. 2011), the alde- hyde reductases belong to SDR family, their catalytic abilities to hyde reductases localized in different organelles may play a pro- aldehydes, the types of catalytic substrates, cofactor prefer- tective role to them by detoxification of endogenous aldehydes. ences, and subcellular localizations were distinct. According to sequence analysis and alignment of cofactor- Based on the enzyme activity analysis of aldehyde reduc- binding sites and active sites, we found that the structure of an tases, it was found that Ari1p, Ydr541cp, and Gre2p not only uncharacterized protein Ykl107wp displayed similar features could catalyze the reduction of furfural (2-furaldehyde, FF) but to Yll056cp and Ykl071wp, and this protein was close to also the reduction of 5-hydroxymethylfurfural (HMF) (Liu and Ykl071wp and Yll056cp in phylogenetic distance (Wang Moon 2009; Moon and Liu 2012, 2015), but Ygl039wp, et al. 2018). Basic Local Alignment Search Tool (BLAST) Yll056cp, and Ykl071wp could only catalyze the reduction re- analysis (https://blast.ncbi.nlm.nih.gov/Blast.cgi)of action of furfural (Moon and Liu 2015;Wangetal.2017a, b). Ykl107wp demonstrates that it is a classical SDR protein Although Ygl039wp, Ari1p, and Ydr541cp catalyzed the reduc- and shares the glycine-rich NAD-binding motif of the classi- tion reactions of propionaldehyde (PA) and isobutyraldehyde cal SDRs. The evidences
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