Deciphering the origin, evolution, and physiological function of the subtelomeric arylalcohol dehydrogenase gene family in the yeast Saccharomyces cerevisiae

Authors

Dong Dong Yang, Université Fédérale Toulouse Midi-Pyrénées
Gustavo M. de Billerbeck, Université Fédérale Toulouse Midi-Pyrénées
Jin Jing Zhang, Zhejiang Agriculture and Forestry University
Frank Rosenzweig, Georgia Institute of Technology
Jean Marie Francois, Université Fédérale Toulouse Midi-Pyrénées

Document Type

Article

Publication Title

Applied and Environmental Microbiology

Publication Date

1-2018

Volume

84

Issue

1

Disciplines

Biology | Life Sciences

Abstract

Homology searches indicate that Saccharomyces cerevisiae strain BY4741 contains seven redundant genes that encode putative aryl-alcohol dehydrogenases (AAD). Yeast AAD genes are located in subtelomeric regions of different chromosomes, and their functional role(s) remain enigmatic. Here, we show that two of these genes, AAD4 and AAD14, encode functional enzymes that reduce aliphatic and aryl-aldehydes concomitant with the oxidation of cofactor NADPH, and that Aad4p and Aad14p exhibit different substrate preference patterns. Other yeast AAD genes are undergoing pseudogenization. The 5' sequence of AAD15 has been deleted from the genome. Repair of an AAD3 missense mutation at the catalytically essential Tyr73 residue did not result in a functional enzyme. However, ancestral-state reconstruction by fusing Aad6 with Aad16 and by N-terminal repair of Aad10 restores NADPHdependent aryl-alcohol dehydrogenase activities. Phylogenetic analysis indicates that AAD genes are narrowly distributed in wood-saprophyte fungi and in yeast that occupy lignocellulosic niches. Because yeast AAD genes exhibit activity on veratraldehyde, cinnamaldehyde, and vanillin, they could serve to detoxify aryl-aldehydes released during lignin degradation. However, none of these compounds induce yeast AAD gene expression, and Aad activities do not relieve aryl-aldehyde growth inhibition. Our data suggest an ancestral role for AAD genes in lignin degradation that is degenerating as a result of yeast's domestication and use in brewing, baking, and other industrial applications.

Keywords

AKR superfamily, Aryl-alcohol dehydrogenases, Evolution, Lignin, Pseudogenization, Subtelomeric

DOI

https://doi.org/10.1128/AEM.01553-17

Rights

© 2017 Yang et al.

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Recommended Citation

Dong-Dong Yang, Gustavo M. de Billerbeck, Jin-jing Zhang, Frank Rosenzweig, Jean-Marie Francois. Applied and Environmental Microbiology Dec 2017, 84 (1) e01553-17; DOI: 10.1128/AEM.01553-17