Discovery and Functional Characterization of a Yeast Sugar Alcohol Phosphatase

Xu, Yi -Fan; Lu, Wenyun; Chen, Jonathan C.; Johnson, Sarah A.; Gibney, Patrick A.; Thomas, David G.; Brown, Greg; May, Amanda L.; Campagna, Shawn R.; Yakunin, Alexander F.; Botstein, David; Rabinowitz, Joshua D.

doi:10.1021/acschembio.8b00804

Title: Discovery and Functional Characterization of a Yeast Sugar Alcohol Phosphatase

Abstract

Sugar alcohols (polyols) exist widely in nature. While some specific sugar alcohol phosphatases are known, there is no known phosphatase for some important sugar alcohols (e.g., sorbitol-6-phosphate). Using liquid chromatography–mass spectrometry-based metabolomics, we screened yeast strains with putative phosphatases of unknown function deleted. We show that the yeast gene YNL010W, which has close homologues in all fungi species and some plants, encodes a sugar alcohol phosphatase. We term this enzyme, which hydrolyzes sorbitol-6-phosphate, ribitol-5-phosphate, and (d)-glycerol-3-phosphate, polyol phosphatase 1 or PYP1. Polyol phosphates are structural analogs of the enediol intermediate of phosphoglucose isomerase (Pgi). We find that sorbitol-6-phosphate and ribitol-5-phosphate inhibit Pgi and that Pyp1 activity is important for yeast to maintain Pgi activity in the presence of environmental sugar alcohols. Pyp1 expression is strongly positively correlated with yeast growth rate, presumably because faster growth requires greater glycolytic and accordingly Pgi flux. Thus, yeast express the previously uncharacterized enzyme Pyp1 to prevent inhibition of glycolysis by sugar alcohol phosphates. Pyp1 may be useful for engineering sugar alcohol production.

Authors:

^[1]; Lu, Wenyun ^[1]; Chen, Jonathan C. ^[1]; Johnson, Sarah A. ^[1]; Gibney, Patrick A. ^[1]; Thomas, David G. ^[1]; Brown, Greg ^[2]; May, Amanda L. ^[3]; Campagna, Shawn R. ^[3];

^[2]; Botstein, David ^[1];

^[1]

Princeton Univ., Princeton, NJ (United States)
Univ. of Toronto, Toronto, ON (Canada)
Univ. of Tennessee, Knoxville, TN (United States)

Publication Date:: 2018-09-21

Research Org.:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1484746

Alternate Identifier(s):: OSTI ID: 1991817

Grant/Contract Number:: SC0018420

Resource Type:: Accepted Manuscript

Journal Name:: ACS Chemical Biology

Additional Journal Information:: Journal Volume: 13; Journal Issue: 10; Journal ID: ISSN 1554-8929

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Xu, Yi -Fan, Lu, Wenyun, Chen, Jonathan C., Johnson, Sarah A., Gibney, Patrick A., Thomas, David G., Brown, Greg, May, Amanda L., Campagna, Shawn R., Yakunin, Alexander F., Botstein, David, and Rabinowitz, Joshua D. Discovery and Functional Characterization of a Yeast Sugar Alcohol Phosphatase.  United States: N. p., 2018. 
Web.  doi:10.1021/acschembio.8b00804.

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                    Xu, Yi -Fan, Lu, Wenyun, Chen, Jonathan C., Johnson, Sarah A., Gibney, Patrick A., Thomas, David G., Brown, Greg, May, Amanda L., Campagna, Shawn R., Yakunin, Alexander F., Botstein, David, & Rabinowitz, Joshua D. Discovery and Functional Characterization of a Yeast Sugar Alcohol Phosphatase.  United States.  https://doi.org/10.1021/acschembio.8b00804

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                    Xu, Yi -Fan, Lu, Wenyun, Chen, Jonathan C., Johnson, Sarah A., Gibney, Patrick A., Thomas, David G., Brown, Greg, May, Amanda L., Campagna, Shawn R., Yakunin, Alexander F., Botstein, David, and Rabinowitz, Joshua D. Fri .  
"Discovery and Functional Characterization of a Yeast Sugar Alcohol Phosphatase".  United States.  https://doi.org/10.1021/acschembio.8b00804.  https://www.osti.gov/servlets/purl/1484746.

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@article{osti_1484746,

  title        = {Discovery and Functional Characterization of a Yeast Sugar Alcohol Phosphatase},

  author       = {Xu, Yi -Fan and Lu, Wenyun and Chen, Jonathan C. and Johnson, Sarah A. and Gibney, Patrick A. and Thomas, David G. and Brown, Greg and May, Amanda L. and Campagna, Shawn R. and Yakunin, Alexander F. and Botstein, David and Rabinowitz, Joshua D.},

  abstractNote = {Sugar alcohols (polyols) exist widely in nature. While some specific sugar alcohol phosphatases are known, there is no known phosphatase for some important sugar alcohols (e.g., sorbitol-6-phosphate). Using liquid chromatography–mass spectrometry-based metabolomics, we screened yeast strains with putative phosphatases of unknown function deleted. We show that the yeast gene YNL010W, which has close homologues in all fungi species and some plants, encodes a sugar alcohol phosphatase. We term this enzyme, which hydrolyzes sorbitol-6-phosphate, ribitol-5-phosphate, and (d)-glycerol-3-phosphate, polyol phosphatase 1 or PYP1. Polyol phosphates are structural analogs of the enediol intermediate of phosphoglucose isomerase (Pgi). We find that sorbitol-6-phosphate and ribitol-5-phosphate inhibit Pgi and that Pyp1 activity is important for yeast to maintain Pgi activity in the presence of environmental sugar alcohols. Pyp1 expression is strongly positively correlated with yeast growth rate, presumably because faster growth requires greater glycolytic and accordingly Pgi flux. Thus, yeast express the previously uncharacterized enzyme Pyp1 to prevent inhibition of glycolysis by sugar alcohol phosphates. Pyp1 may be useful for engineering sugar alcohol production.},

  doi          = {10.1021/acschembio.8b00804},

  journal      = {ACS Chemical Biology},

  number       = 10,

  volume       = 13,

  place        = {United States},

  year         = {2018},

  month        = {9}

}

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