Global analysis and comparison of the transcriptomes and proteomes of group a Streptococcus biofilms

Jeffrey A. Freiberg; Yoann Le Breton; Bao Q. Tran; Alison J. Scott; Janette M. Harro; Robert K. Ernst; Young Ah Goo; Emmanuel F. Mongodin; David R. Goodlett; Kevin S. McIver; Mark E. Shirtliff

doi:10.1128/mSystems.00149-16

Global analysis and comparison of the transcriptomes and proteomes of group a Streptococcus biofilms

Jeffrey A. Freiberg, Yoann Le Breton, Bao Q. Tran, Alison J. Scott, Janette M. Harro, Robert K. Ernst, Young Ah Goo, Emmanuel F. Mongodin, David R. Goodlett, Kevin S. McIver, Mark E. Shirtliff^*

^*Corresponding author for this work

PCE - Proteomics Center of Excellence

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

27 Scopus citations

Abstract

To gain a better understanding of the genes and proteins involved in group A Streptococcus (GAS; Streptococcus pyogenes) biofilm growth, we analyzed the transcriptome, cellular proteome, and cell wall proteome from biofilms at different stages and compared them to those of plankton-stage GAS. Using high-throughput RNA sequencing (RNA-seq) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) shotgun proteomics, we found distinct expression profiles in the transcriptome and proteome. A total of 46 genes and 41 proteins showed expression across the majority of biofilm time points that was consistently higher or consistently lower than that seen across the majority of planktonic time points. However, there was little overlap between the genes and proteins on these two lists. In line with other studies comparing transcriptomic and proteomic data, the overall correlation between the two data sets was modest. Furthermore, correlation was poorest for biofilm samples. This suggests a high degree of regulation of protein expression by nontranscriptional mechanisms. This report illustrates the benefits and weaknesses of two different approaches to global expression profiling, and it also demonstrates the advantage of using proteomics in conjunction with transcriptomics to gain a more complete picture of global expression within biofilms. In addition, this report provides the fullest characterization of expression patterns in GAS biofilms currently available.

Original language	English (US)
Article number	e00149
Journal	mSystems
Volume	1
Issue number	6
DOIs	https://doi.org/10.1128/mSystems.00149-16
State	Published - Nov 1 2016

Funding

This work, including the efforts of Yoann Le Breton, Kevin S. McIver, and Mark E. Shirtliff, was funded by University of Maryland, Baltimore/University of Maryland, College Park Seed Grant. This work, including the efforts of Mark E. Shirtliff, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI069568). This work, including the efforts of Kevin S. McIver, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI047928). This work, including the efforts of Jeffrey A. Freiberg and Alison J. Scott, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (T32AI007540). We thank Emrul Islam for exceptional technical assistance. We also thank Daniel Nelson for providing the PlyC lysin and Matak Kotb for providing the SpeB antibody used in this study. This work, including the efforts of Yoann Le Breton, Kevin S. McIver, and Mark E. Shirtliff, was funded by University of Maryland, Baltimore/University of Maryland, College Park Seed Grant. This work, including the efforts of Mark E. Shirtliff, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI069568). This work, including the efforts of Kevin S. McIver, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI047928). This work, including the efforts of Jeffrey A. Freiberg and Alison J. Scott, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (T32AI007540).

Keywords

LC-MS/MS
RNA-seq
Shotgun proteomics
Streptococcus pyogenes
Transcriptomics

ASJC Scopus subject areas

Microbiology
Physiology
Biochemistry
Ecology, Evolution, Behavior and Systematics
Modeling and Simulation
Molecular Biology
Genetics
Computer Science Applications

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10.1128/mSystems.00149-16

Cite this

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title = "Global analysis and comparison of the transcriptomes and proteomes of group a Streptococcus biofilms",

abstract = "To gain a better understanding of the genes and proteins involved in group A Streptococcus (GAS; Streptococcus pyogenes) biofilm growth, we analyzed the transcriptome, cellular proteome, and cell wall proteome from biofilms at different stages and compared them to those of plankton-stage GAS. Using high-throughput RNA sequencing (RNA-seq) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) shotgun proteomics, we found distinct expression profiles in the transcriptome and proteome. A total of 46 genes and 41 proteins showed expression across the majority of biofilm time points that was consistently higher or consistently lower than that seen across the majority of planktonic time points. However, there was little overlap between the genes and proteins on these two lists. In line with other studies comparing transcriptomic and proteomic data, the overall correlation between the two data sets was modest. Furthermore, correlation was poorest for biofilm samples. This suggests a high degree of regulation of protein expression by nontranscriptional mechanisms. This report illustrates the benefits and weaknesses of two different approaches to global expression profiling, and it also demonstrates the advantage of using proteomics in conjunction with transcriptomics to gain a more complete picture of global expression within biofilms. In addition, this report provides the fullest characterization of expression patterns in GAS biofilms currently available.",

keywords = "LC-MS/MS, RNA-seq, Shotgun proteomics, Streptococcus pyogenes, Transcriptomics",

author = "Freiberg, {Jeffrey A.} and {Le Breton}, Yoann and Tran, {Bao Q.} and Scott, {Alison J.} and Harro, {Janette M.} and Ernst, {Robert K.} and Goo, {Young Ah} and Mongodin, {Emmanuel F.} and Goodlett, {David R.} and McIver, {Kevin S.} and Shirtliff, {Mark E.}",

note = "Funding Information: This work, including the efforts of Yoann Le Breton, Kevin S. McIver, and Mark E. Shirtliff, was funded by University of Maryland, Baltimore/University of Maryland, College Park Seed Grant. This work, including the efforts of Mark E. Shirtliff, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI069568). This work, including the efforts of Kevin S. McIver, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI047928). This work, including the efforts of Jeffrey A. Freiberg and Alison J. Scott, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (T32AI007540). Funding Information: We thank Emrul Islam for exceptional technical assistance. We also thank Daniel Nelson for providing the PlyC lysin and Matak Kotb for providing the SpeB antibody used in this study. This work, including the efforts of Yoann Le Breton, Kevin S. McIver, and Mark E. Shirtliff, was funded by University of Maryland, Baltimore/University of Maryland, College Park Seed Grant. This work, including the efforts of Mark E. Shirtliff, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI069568). This work, including the efforts of Kevin S. McIver, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI047928). This work, including the efforts of Jeffrey A. Freiberg and Alison J. Scott, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (T32AI007540). Publisher Copyright: Copyright {\textcopyright} 2016 Freiberg et al.",

year = "2016",

month = nov,

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doi = "10.1128/mSystems.00149-16",

language = "English (US)",

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AU - Freiberg, Jeffrey A.

AU - Le Breton, Yoann

AU - Tran, Bao Q.

AU - Scott, Alison J.

AU - Harro, Janette M.

AU - Ernst, Robert K.

AU - Goo, Young Ah

AU - Mongodin, Emmanuel F.

AU - Goodlett, David R.

AU - McIver, Kevin S.

AU - Shirtliff, Mark E.

N1 - Funding Information: This work, including the efforts of Yoann Le Breton, Kevin S. McIver, and Mark E. Shirtliff, was funded by University of Maryland, Baltimore/University of Maryland, College Park Seed Grant. This work, including the efforts of Mark E. Shirtliff, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI069568). This work, including the efforts of Kevin S. McIver, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI047928). This work, including the efforts of Jeffrey A. Freiberg and Alison J. Scott, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (T32AI007540). Funding Information: We thank Emrul Islam for exceptional technical assistance. We also thank Daniel Nelson for providing the PlyC lysin and Matak Kotb for providing the SpeB antibody used in this study. This work, including the efforts of Yoann Le Breton, Kevin S. McIver, and Mark E. Shirtliff, was funded by University of Maryland, Baltimore/University of Maryland, College Park Seed Grant. This work, including the efforts of Mark E. Shirtliff, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI069568). This work, including the efforts of Kevin S. McIver, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (R01AI047928). This work, including the efforts of Jeffrey A. Freiberg and Alison J. Scott, was funded by HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID) (T32AI007540). Publisher Copyright: Copyright © 2016 Freiberg et al.

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N2 - To gain a better understanding of the genes and proteins involved in group A Streptococcus (GAS; Streptococcus pyogenes) biofilm growth, we analyzed the transcriptome, cellular proteome, and cell wall proteome from biofilms at different stages and compared them to those of plankton-stage GAS. Using high-throughput RNA sequencing (RNA-seq) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) shotgun proteomics, we found distinct expression profiles in the transcriptome and proteome. A total of 46 genes and 41 proteins showed expression across the majority of biofilm time points that was consistently higher or consistently lower than that seen across the majority of planktonic time points. However, there was little overlap between the genes and proteins on these two lists. In line with other studies comparing transcriptomic and proteomic data, the overall correlation between the two data sets was modest. Furthermore, correlation was poorest for biofilm samples. This suggests a high degree of regulation of protein expression by nontranscriptional mechanisms. This report illustrates the benefits and weaknesses of two different approaches to global expression profiling, and it also demonstrates the advantage of using proteomics in conjunction with transcriptomics to gain a more complete picture of global expression within biofilms. In addition, this report provides the fullest characterization of expression patterns in GAS biofilms currently available.

AB - To gain a better understanding of the genes and proteins involved in group A Streptococcus (GAS; Streptococcus pyogenes) biofilm growth, we analyzed the transcriptome, cellular proteome, and cell wall proteome from biofilms at different stages and compared them to those of plankton-stage GAS. Using high-throughput RNA sequencing (RNA-seq) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) shotgun proteomics, we found distinct expression profiles in the transcriptome and proteome. A total of 46 genes and 41 proteins showed expression across the majority of biofilm time points that was consistently higher or consistently lower than that seen across the majority of planktonic time points. However, there was little overlap between the genes and proteins on these two lists. In line with other studies comparing transcriptomic and proteomic data, the overall correlation between the two data sets was modest. Furthermore, correlation was poorest for biofilm samples. This suggests a high degree of regulation of protein expression by nontranscriptional mechanisms. This report illustrates the benefits and weaknesses of two different approaches to global expression profiling, and it also demonstrates the advantage of using proteomics in conjunction with transcriptomics to gain a more complete picture of global expression within biofilms. In addition, this report provides the fullest characterization of expression patterns in GAS biofilms currently available.

KW - LC-MS/MS

KW - RNA-seq

KW - Shotgun proteomics

KW - Streptococcus pyogenes

KW - Transcriptomics

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Global analysis and comparison of the transcriptomes and proteomes of group a Streptococcus biofilms

Abstract

Funding

Keywords

ASJC Scopus subject areas

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