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Title: Identification of Novel Protein Lysine Acetyltransferases in Escherichia coli

Abstract

ABSTRACT Posttranslational modifications, such asNε-lysine acetylation, regulate protein function.Nε-lysine acetylation can occur either nonenzymatically or enzymatically. The nonenzymatic mechanism uses acetyl phosphate (AcP) or acetyl coenzyme A (AcCoA) as acetyl donor to modify anNε-lysine residue of a protein. The enzymatic mechanism usesNε-lysine acetyltransferases (KATs) to specifically transfer an acetyl group from AcCoA toNε-lysine residues on proteins. To date, only one KAT (YfiQ, also known as Pka and PatZ) has been identified inEscherichia coli. Here, we demonstrate the existence of 4 additionalE. coliKATs: RimI, YiaC, YjaB, and PhnO. In a genetic background devoid of all known acetylation mechanisms (most notably AcP and YfiQ) and one deacetylase (CobB), overexpression of these putative KATs elicited unique patterns of protein acetylation. We mutated key active site residues and found that most of them eliminated enzymatic acetylation activity. We used mass spectrometry to identify and quantify the specificity of YfiQ and the four novel KATs. Surprisingly, our analysis revealed a high degree of substrate specificity. The overlap among KAT-dependent and AcP-dependent acetylation was extremely limited, supporting the hypothesis that these two acetylation mechanisms play distinct roles in the posttranslational modification of bacterial proteins. We alos showed that these novel KATs are conserved across broad swathsmore » of bacterial phylogeny. Lastly, we determined that one of the novel KATs (YiaC) and the known KAT (YfiQ) can negatively regulate bacterial migration. Together, these results emphasize distinct and specific nonenzymatic and enzymatic protein acetylation mechanisms present in bacteria. IMPORTANCE Nε-Lysine acetylation is one of the most abundant and important posttranslational modifications across all domains of life. One of the best-studied effects of acetylation occurs in eukaryotes, where acetylation of histone tails activates gene transcription. Although bacteria do not have true histones,Nε-lysine acetylation is prevalent; however, the role of these modifications is mostly unknown. We constructed anE. colistrain that lacked both known acetylation mechanisms to identify four newNε-lysine acetyltransferases (RimI, YiaC, YjaB, and PhnO). We used mass spectrometry to determine the substrate specificity of these acetyltransferases. Structural analysis of selected substrate proteins revealed site-specific preferences for enzymatic acetylation that had little overlap with the preferences of the previously reported acetyl-phosphate nonenzymatic acetylation mechanism. Finally, YiaC and YfiQ appear to regulate flagellum-based motility, a phenotype critical for pathogenesis of many organisms. These acetyltransferases are highly conserved and reveal deeper and more complex roles for bacterial posttranslational modification.« less

Authors:
ORCiD logo [1];  [2];  [3];  [2]; ORCiD logo [4]; ORCiD logo [4];  [3];  [2];  [2];  [5]
+ Show Author Affiliations
  1. Loyola Univ., Maywood, IL (United States)
  2. Buck Inst. for Research on Aging, Novato, CA (United States)
  3. San Francisco State Univ., CA (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  5. Univ. of Illinois, Chicago, IL (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE; National Institutes of Health (NIH)
OSTI Identifier:
1558369
Report Number(s):
PNNL-SA-138542
Journal ID: ISSN 2150-7511
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 9; Journal Issue: 5; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; BACTERIA; acetylation; acetyltransferase; GNAT; Mass spectrometry (MS); proteomics; protein acetylation

Citation Formats

Christensen, David G., Meyer, Jesse G., Baumgartner, Jackson T., D’Souza, Alexandria K., Nelson, William C., Payne, Samuel H., Kuhn, Misty L., Schilling, Birgit, Wolfe, Alan J., and Freitag, Nancy E. Identification of Novel Protein Lysine Acetyltransferases in Escherichia coli. United States: N. p., 2018. Web. doi:10.1128/mBio.01905-18.
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Christensen, David G., Meyer, Jesse G., Baumgartner, Jackson T., D’Souza, Alexandria K., Nelson, William C., Payne, Samuel H., Kuhn, Misty L., Schilling, Birgit, Wolfe, Alan J., & Freitag, Nancy E. Identification of Novel Protein Lysine Acetyltransferases in Escherichia coli. United States. https://doi.org/10.1128/mBio.01905-18
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Christensen, David G., Meyer, Jesse G., Baumgartner, Jackson T., D’Souza, Alexandria K., Nelson, William C., Payne, Samuel H., Kuhn, Misty L., Schilling, Birgit, Wolfe, Alan J., and Freitag, Nancy E. Tue . "Identification of Novel Protein Lysine Acetyltransferases in Escherichia coli". United States. https://doi.org/10.1128/mBio.01905-18. https://www.osti.gov/servlets/purl/1558369.
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@article{osti_1558369,
title = {Identification of Novel Protein Lysine Acetyltransferases in Escherichia coli},
author = {Christensen, David G. and Meyer, Jesse G. and Baumgartner, Jackson T. and D’Souza, Alexandria K. and Nelson, William C. and Payne, Samuel H. and Kuhn, Misty L. and Schilling, Birgit and Wolfe, Alan J. and Freitag, Nancy E.},
abstractNote = {ABSTRACT Posttranslational modifications, such asNε-lysine acetylation, regulate protein function.Nε-lysine acetylation can occur either nonenzymatically or enzymatically. The nonenzymatic mechanism uses acetyl phosphate (AcP) or acetyl coenzyme A (AcCoA) as acetyl donor to modify anNε-lysine residue of a protein. The enzymatic mechanism usesNε-lysine acetyltransferases (KATs) to specifically transfer an acetyl group from AcCoA toNε-lysine residues on proteins. To date, only one KAT (YfiQ, also known as Pka and PatZ) has been identified inEscherichia coli. Here, we demonstrate the existence of 4 additionalE. coliKATs: RimI, YiaC, YjaB, and PhnO. In a genetic background devoid of all known acetylation mechanisms (most notably AcP and YfiQ) and one deacetylase (CobB), overexpression of these putative KATs elicited unique patterns of protein acetylation. We mutated key active site residues and found that most of them eliminated enzymatic acetylation activity. We used mass spectrometry to identify and quantify the specificity of YfiQ and the four novel KATs. Surprisingly, our analysis revealed a high degree of substrate specificity. The overlap among KAT-dependent and AcP-dependent acetylation was extremely limited, supporting the hypothesis that these two acetylation mechanisms play distinct roles in the posttranslational modification of bacterial proteins. We alos showed that these novel KATs are conserved across broad swaths of bacterial phylogeny. Lastly, we determined that one of the novel KATs (YiaC) and the known KAT (YfiQ) can negatively regulate bacterial migration. Together, these results emphasize distinct and specific nonenzymatic and enzymatic protein acetylation mechanisms present in bacteria. IMPORTANCE Nε-Lysine acetylation is one of the most abundant and important posttranslational modifications across all domains of life. One of the best-studied effects of acetylation occurs in eukaryotes, where acetylation of histone tails activates gene transcription. Although bacteria do not have true histones,Nε-lysine acetylation is prevalent; however, the role of these modifications is mostly unknown. We constructed anE. colistrain that lacked both known acetylation mechanisms to identify four newNε-lysine acetyltransferases (RimI, YiaC, YjaB, and PhnO). We used mass spectrometry to determine the substrate specificity of these acetyltransferases. Structural analysis of selected substrate proteins revealed site-specific preferences for enzymatic acetylation that had little overlap with the preferences of the previously reported acetyl-phosphate nonenzymatic acetylation mechanism. Finally, YiaC and YfiQ appear to regulate flagellum-based motility, a phenotype critical for pathogenesis of many organisms. These acetyltransferases are highly conserved and reveal deeper and more complex roles for bacterial posttranslational modification.},
doi = {10.1128/mBio.01905-18},
journal = {mBio (Online)},
number = 5,
volume = 9,
place = {United States},
year = {Tue Oct 23 00:00:00 EDT 2018},
month = {Tue Oct 23 00:00:00 EDT 2018}
}
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Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli.
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