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Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor.

Jayapal KP, Philp RJ, Kok YJ, Yap MG, Sherman DH, Griffin TJ, Hu WS - PLoS ONE (2008)

Bottom Line: Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels.Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends.Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical Engineering and Materials Science, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels. Systems analyses of such processes incorporating large-scale transcriptome or proteome profiling can be quite revealing. Although consistency between mRNA and proteins is often implicitly assumed in many studies, examples of divergent trends are frequently observed. Here, we present a comparative transcriptome and proteome analysis of growth and stationary phase adaptation in Streptomyces coelicolor, taking the time-dynamics of process into consideration. These processes are of immense interest in microbiology as they pertain to the physiological transformations eliciting biosynthesis of many naturally occurring therapeutic agents. A shotgun proteomics approach based on mass spectrometric analysis of isobaric stable isotope labeled peptides (iTRAQ) enabled identification and rapid quantification of approximately 14% of the theoretical proteome of S. coelicolor. Independent principal component analyses of this and DNA microarray-derived transcriptome data revealed that the prominent patterns in both protein and mRNA domains are surprisingly well correlated. Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends. Integrating this data with biological information, we discovered that certain groups of functionally related genes exhibit mRNA-protein discordance in a similar fashion. Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

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Growth-time curve of S. coelicolor in R5− complex media.Samples analyzed by MS runs 1, 2 and 3 are indicated.
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pone-0002097-g001: Growth-time curve of S. coelicolor in R5− complex media.Samples analyzed by MS runs 1, 2 and 3 are indicated.

Mentions: To examine the changes in proteome profiles associated with growth and adaptation in S. coelicolor M145 cells, we isolated total cell proteins from eight temporally spaced samples (7 h, 11 h, 14 h, 16 h, 22 h, 26 h, 34 h and 38 h) as shown in Figure 1. The samples chosen reflect changes in cellular physiology associated with growth and transition to stationary phase as well as the conspicuous onsets of two prominent antibiotics, undecylprodigiosin and actinorhodin. Since the iTRAQ™ system used in this study can analyze only four distinct samples in a single experiment, we chose to distribute the eight protein samples to three runs of mass spectrometric analysis (Figure 1). The experiments were also designed so as to enable validation of the methodology by comparison of two protein ratios (16 h/11 h and 38 h/11 h) estimated from independent replicate runs.


Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor.

Jayapal KP, Philp RJ, Kok YJ, Yap MG, Sherman DH, Griffin TJ, Hu WS - PLoS ONE (2008)

Growth-time curve of S. coelicolor in R5− complex media.Samples analyzed by MS runs 1, 2 and 3 are indicated.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2367054&req=5

pone-0002097-g001: Growth-time curve of S. coelicolor in R5− complex media.Samples analyzed by MS runs 1, 2 and 3 are indicated.
Mentions: To examine the changes in proteome profiles associated with growth and adaptation in S. coelicolor M145 cells, we isolated total cell proteins from eight temporally spaced samples (7 h, 11 h, 14 h, 16 h, 22 h, 26 h, 34 h and 38 h) as shown in Figure 1. The samples chosen reflect changes in cellular physiology associated with growth and transition to stationary phase as well as the conspicuous onsets of two prominent antibiotics, undecylprodigiosin and actinorhodin. Since the iTRAQ™ system used in this study can analyze only four distinct samples in a single experiment, we chose to distribute the eight protein samples to three runs of mass spectrometric analysis (Figure 1). The experiments were also designed so as to enable validation of the methodology by comparison of two protein ratios (16 h/11 h and 38 h/11 h) estimated from independent replicate runs.

Bottom Line: Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels.Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends.Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemical Engineering and Materials Science, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
Many biological processes are intrinsically dynamic, incurring profound changes at both molecular and physiological levels. Systems analyses of such processes incorporating large-scale transcriptome or proteome profiling can be quite revealing. Although consistency between mRNA and proteins is often implicitly assumed in many studies, examples of divergent trends are frequently observed. Here, we present a comparative transcriptome and proteome analysis of growth and stationary phase adaptation in Streptomyces coelicolor, taking the time-dynamics of process into consideration. These processes are of immense interest in microbiology as they pertain to the physiological transformations eliciting biosynthesis of many naturally occurring therapeutic agents. A shotgun proteomics approach based on mass spectrometric analysis of isobaric stable isotope labeled peptides (iTRAQ) enabled identification and rapid quantification of approximately 14% of the theoretical proteome of S. coelicolor. Independent principal component analyses of this and DNA microarray-derived transcriptome data revealed that the prominent patterns in both protein and mRNA domains are surprisingly well correlated. Despite this overall correlation, by employing a systematic concordance analysis, we estimated that over 30% of the analyzed genes likely exhibited significantly divergent patterns, of which nearly one-third displayed even opposing trends. Integrating this data with biological information, we discovered that certain groups of functionally related genes exhibit mRNA-protein discordance in a similar fashion. Our observations suggest that differences between mRNA and protein synthesis/degradation mechanisms are prominent in microbes while reaffirming the plausibility of such mechanisms acting in a concerted fashion at a protein complex or sub-pathway level.

Show MeSH
Related in: MedlinePlus