Transcriptional profiling and molecular characterization of the yccT mutant link: A novel STY1099 protein with the peroxide stress response and cell division of Salmonella enterica serovar enteritidis

Sinisa Vidovic; Xiaoying Liu; Ran An; Kristelle M. Mendoza; Juan E. Abrahante; Anup K. Johny; Kent M. Reed

doi:10.3390/biology8040086

Transcriptional profiling and molecular characterization of the yccT mutant link: A novel STY1099 protein with the peroxide stress response and cell division of Salmonella enterica serovar enteritidis

Sinisa Vidovic, Xiaoying Liu, Ran An, Kristelle M. Mendoza, Juan E. Abrahante, Anup K. Johny, Kent M. Reed

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Uncharacterized protein STY1099, encoded by the yccT gene, was previously identified as the most altered (i.e., upregulated) protein among the ZnO nanoparticle (NP) stimulon of Salmonella enterica serovar Enteritidis. Here we combined various stress response-related assays with functional genetics, global transcriptomic and proteomic analyses to characterize the yccT gene and its STY1099 product. Exposure of S. enterica Enteritidis to H2O2 (i.e., hydrogen peroxide) resulted in a significant (p < 0.0001) upregulation of the yccT gene, whereas exposure to paraquat (i.e., superoxide) did not alter the expression of the yccT gene. The ∆yccT mutant of S. enterica Enteritidis exposed to 0.75 mM H2O2, showed significantly reduced (p < 0.05) viability compared to the wild type strain. Further, comparative transcriptome analyses supported by Co-immunoprecipitation (Co-IP) assay revealed that STY1099 protein plays a role in redox homeostasis during the peroxide stress assault via involvement in the processes of respiratory nitrate reductase, oxidoreductase activities, cellular uptake and stress response. In addition, we found that the STY1099 protein has the monopolar subcellular location and that it interacts with key cell division proteins, MinD, and FtsH, as well as with a rod shape-determining protein MerB.

Original language	English (US)
Article number	86
Journal	Biology
Volume	8
Issue number	4
DOIs	https://doi.org/10.3390/biology8040086
State	Published - Dec 2019

Bibliographical note

Funding Information:
Acknowledgments: The authors gratefully acknowledge the technical support from the University Imaging Centers at the University of Minnesota, Jim Imlay, Sergei Korshunov and Daniela Vidovic. We also thank Misara Omar and Sahar Alshalchi for their assistance. This project was supported by the Signature Program AES GAR grant. The present study was also supported, in part, by resources provided by the Minnesota Supercomputing Institute.

Funding Information:
Funding: This research was funded by the United States Department of Agriculture, National Institute of Food and Agriculture, Hatch Capacity Grant # 592 and Grant-in-Aid of Research, Artistry and Scholarship, University of Minnesota, USA to S.V.

Publisher Copyright:
© 2019 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Cell division
Nitrate reductase
Peroxide stress response
STY1099 protein
Salmonella enterica serovar Enteritidis

Access

10.3390/biology8040086

OpenUrl availability

Full text

Cite this

@article{d61fbbaed4cd4d57b7e7a9db868e87a4,

title = "Transcriptional profiling and molecular characterization of the yccT mutant link: A novel STY1099 protein with the peroxide stress response and cell division of Salmonella enterica serovar enteritidis",

abstract = "Uncharacterized protein STY1099, encoded by the yccT gene, was previously identified as the most altered (i.e., upregulated) protein among the ZnO nanoparticle (NP) stimulon of Salmonella enterica serovar Enteritidis. Here we combined various stress response-related assays with functional genetics, global transcriptomic and proteomic analyses to characterize the yccT gene and its STY1099 product. Exposure of S. enterica Enteritidis to H2O2 (i.e., hydrogen peroxide) resulted in a significant (p < 0.0001) upregulation of the yccT gene, whereas exposure to paraquat (i.e., superoxide) did not alter the expression of the yccT gene. The ∆yccT mutant of S. enterica Enteritidis exposed to 0.75 mM H2O2, showed significantly reduced (p < 0.05) viability compared to the wild type strain. Further, comparative transcriptome analyses supported by Co-immunoprecipitation (Co-IP) assay revealed that STY1099 protein plays a role in redox homeostasis during the peroxide stress assault via involvement in the processes of respiratory nitrate reductase, oxidoreductase activities, cellular uptake and stress response. In addition, we found that the STY1099 protein has the monopolar subcellular location and that it interacts with key cell division proteins, MinD, and FtsH, as well as with a rod shape-determining protein MerB.",

keywords = "Cell division, Nitrate reductase, Peroxide stress response, STY1099 protein, Salmonella enterica serovar Enteritidis",

author = "Sinisa Vidovic and Xiaoying Liu and Ran An and Mendoza, {Kristelle M.} and Abrahante, {Juan E.} and Johny, {Anup K.} and Reed, {Kent M.}",

note = "Funding Information: Acknowledgments: The authors gratefully acknowledge the technical support from the University Imaging Centers at the University of Minnesota, Jim Imlay, Sergei Korshunov and Daniela Vidovic. We also thank Misara Omar and Sahar Alshalchi for their assistance. This project was supported by the Signature Program AES GAR grant. The present study was also supported, in part, by resources provided by the Minnesota Supercomputing Institute. Funding Information: Funding: This research was funded by the United States Department of Agriculture, National Institute of Food and Agriculture, Hatch Capacity Grant # 592 and Grant-in-Aid of Research, Artistry and Scholarship, University of Minnesota, USA to S.V. Publisher Copyright: {\textcopyright} 2019 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2019",

month = dec,

doi = "10.3390/biology8040086",

language = "English (US)",

volume = "8",

journal = "Biology",

issn = "2079-7737",

publisher = "Multidisciplinary Digital Publishing Institute (MDPI)",

number = "4",

}

TY - JOUR

T1 - Transcriptional profiling and molecular characterization of the yccT mutant link

T2 - A novel STY1099 protein with the peroxide stress response and cell division of Salmonella enterica serovar enteritidis

AU - Vidovic, Sinisa

AU - Liu, Xiaoying

AU - An, Ran

AU - Mendoza, Kristelle M.

AU - Abrahante, Juan E.

AU - Johny, Anup K.

AU - Reed, Kent M.

N1 - Funding Information: Acknowledgments: The authors gratefully acknowledge the technical support from the University Imaging Centers at the University of Minnesota, Jim Imlay, Sergei Korshunov and Daniela Vidovic. We also thank Misara Omar and Sahar Alshalchi for their assistance. This project was supported by the Signature Program AES GAR grant. The present study was also supported, in part, by resources provided by the Minnesota Supercomputing Institute. Funding Information: Funding: This research was funded by the United States Department of Agriculture, National Institute of Food and Agriculture, Hatch Capacity Grant # 592 and Grant-in-Aid of Research, Artistry and Scholarship, University of Minnesota, USA to S.V. Publisher Copyright: © 2019 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2019/12

Y1 - 2019/12

N2 - Uncharacterized protein STY1099, encoded by the yccT gene, was previously identified as the most altered (i.e., upregulated) protein among the ZnO nanoparticle (NP) stimulon of Salmonella enterica serovar Enteritidis. Here we combined various stress response-related assays with functional genetics, global transcriptomic and proteomic analyses to characterize the yccT gene and its STY1099 product. Exposure of S. enterica Enteritidis to H2O2 (i.e., hydrogen peroxide) resulted in a significant (p < 0.0001) upregulation of the yccT gene, whereas exposure to paraquat (i.e., superoxide) did not alter the expression of the yccT gene. The ∆yccT mutant of S. enterica Enteritidis exposed to 0.75 mM H2O2, showed significantly reduced (p < 0.05) viability compared to the wild type strain. Further, comparative transcriptome analyses supported by Co-immunoprecipitation (Co-IP) assay revealed that STY1099 protein plays a role in redox homeostasis during the peroxide stress assault via involvement in the processes of respiratory nitrate reductase, oxidoreductase activities, cellular uptake and stress response. In addition, we found that the STY1099 protein has the monopolar subcellular location and that it interacts with key cell division proteins, MinD, and FtsH, as well as with a rod shape-determining protein MerB.

AB - Uncharacterized protein STY1099, encoded by the yccT gene, was previously identified as the most altered (i.e., upregulated) protein among the ZnO nanoparticle (NP) stimulon of Salmonella enterica serovar Enteritidis. Here we combined various stress response-related assays with functional genetics, global transcriptomic and proteomic analyses to characterize the yccT gene and its STY1099 product. Exposure of S. enterica Enteritidis to H2O2 (i.e., hydrogen peroxide) resulted in a significant (p < 0.0001) upregulation of the yccT gene, whereas exposure to paraquat (i.e., superoxide) did not alter the expression of the yccT gene. The ∆yccT mutant of S. enterica Enteritidis exposed to 0.75 mM H2O2, showed significantly reduced (p < 0.05) viability compared to the wild type strain. Further, comparative transcriptome analyses supported by Co-immunoprecipitation (Co-IP) assay revealed that STY1099 protein plays a role in redox homeostasis during the peroxide stress assault via involvement in the processes of respiratory nitrate reductase, oxidoreductase activities, cellular uptake and stress response. In addition, we found that the STY1099 protein has the monopolar subcellular location and that it interacts with key cell division proteins, MinD, and FtsH, as well as with a rod shape-determining protein MerB.

KW - Cell division

KW - Nitrate reductase

KW - Peroxide stress response

KW - STY1099 protein

KW - Salmonella enterica serovar Enteritidis

UR - http://www.scopus.com/inward/record.url?scp=85075282098&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85075282098&partnerID=8YFLogxK

U2 - 10.3390/biology8040086

DO - 10.3390/biology8040086

M3 - Article

C2 - 31766267

AN - SCOPUS:85075282098

SN - 2079-7737

VL - 8

JO - Biology

JF - Biology

IS - 4

M1 - 86

ER -

Transcriptional profiling and molecular characterization of the yccT mutant link: A novel STY1099 protein with the peroxide stress response and cell division of Salmonella enterica serovar enteritidis

Abstract

Bibliographical note

Keywords

Access

OpenUrl availability

Other files and links

Fingerprint

Cite this