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Perceiving molecular evolution processes in Escherichia coli by comprehensive metabolite and gene expression profiling.

Vijayendran C, Barsch A, Friehs K, Niehaus K, Becker A, Flaschel E - Genome Biol. (2008)

Bottom Line: Excess nutrient adapted lines were found to exhibit greater degrees of positive correlation, indicating parallelism between ancestor and evolved lines, when compared with prolonged stationary phase adapted lines.Gene-metabolite correlation network analysis revealed over-representation of membrane-associated functional categories.GltB, LamB and YaeT proteins in excess nutrient lines, and FepA, CirA, OmpC and OmpA in prolonged stationary phase lines were found to be differentially over-expressed.

View Article: PubMed Central - HTML - PubMed

Affiliation: International NRW Graduate School in Bioinformatics and Genome Research, Bielefeld University, D-33594 Bielefeld, Germany. cvijayen@cebitec.uni-bielefeld.de

ABSTRACT

Background: Evolutionary changes that are due to different environmental conditions can be examined based on the various molecular aspects that constitute a cell, namely transcript, protein, or metabolite abundance. We analyzed changes in transcript and metabolite abundance in evolved and ancestor strains in three different evolutionary conditions - excess nutrient adaptation, prolonged stationary phase adaptation, and adaptation because of environmental shift - in two different strains of bacterium Escherichia coli K-12 (MG1655 and DH10B).

Results: Metabolite profiling of 84 identified metabolites revealed that most of the metabolites involved in the tricarboxylic acid cycle and nucleotide metabolism were altered in both of the excess nutrient evolved lines. Gene expression profiling using whole genome microarray with 4,288 open reading frames revealed over-representation of the transport functional category in all evolved lines. Excess nutrient adapted lines were found to exhibit greater degrees of positive correlation, indicating parallelism between ancestor and evolved lines, when compared with prolonged stationary phase adapted lines. Gene-metabolite correlation network analysis revealed over-representation of membrane-associated functional categories. Proteome analysis revealed the major role played by outer membrane proteins in adaptive evolution. GltB, LamB and YaeT proteins in excess nutrient lines, and FepA, CirA, OmpC and OmpA in prolonged stationary phase lines were found to be differentially over-expressed.

Conclusion: In summary, we report the vital involvement of energy metabolism and membrane-associated functional categories in all of the evolutionary conditions examined in this study within the context of transcript, outer membrane protein, and metabolite levels. These initial data obtained may help to enhance our understanding of the evolutionary process from a systems biology perspective.

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Parallelism and functional significance in the outer membrane protein expression. SDS gel electrophoresis of the protein samples obtained from the outer membrane of the ancestor and evolved lines showing the identified proteins by peptide mass fingerprinting.
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Figure 8: Parallelism and functional significance in the outer membrane protein expression. SDS gel electrophoresis of the protein samples obtained from the outer membrane of the ancestor and evolved lines showing the identified proteins by peptide mass fingerprinting.

Mentions: To further examine the extent of parallel evolutionary changes, we determined the expression levels of proteins associated with the outer membrane (OM) of the ancestor and evolved strains, whose membrane-related GO functional categories were over-represented in the evolution-specific co-expression networks (Figure 7a-f). OM protein levels revealed substantial differential expression among the ancestor and evolved strains (Figure 8). In Adp lines, GltB (glutamate synthase [nicotinamide adenine dinucleotide phosphate (NADPH)] large chain precursor), LamB (maltose high-affinity receptor), and YaeT (polypeptide involved in outer-membrane protein biogenesis) proteins were over-expressed; whereas in Stat lines FepA (outer receptor for ferric enterobactin), CirA (outer membrane receptor for iron-regulated colicin I receptor), OmpC (outer membrane porin), and OmpA (outer-membrane porin) proteins were differentially over-expressed (Figure 8). Significantly, we observed parallelism in the level of protein expression patterns in these evolved strains and involvement of the outer membrane proteins in these evolutionary processes.


Perceiving molecular evolution processes in Escherichia coli by comprehensive metabolite and gene expression profiling.

Vijayendran C, Barsch A, Friehs K, Niehaus K, Becker A, Flaschel E - Genome Biol. (2008)

Parallelism and functional significance in the outer membrane protein expression. SDS gel electrophoresis of the protein samples obtained from the outer membrane of the ancestor and evolved lines showing the identified proteins by peptide mass fingerprinting.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2643943&req=5

Figure 8: Parallelism and functional significance in the outer membrane protein expression. SDS gel electrophoresis of the protein samples obtained from the outer membrane of the ancestor and evolved lines showing the identified proteins by peptide mass fingerprinting.
Mentions: To further examine the extent of parallel evolutionary changes, we determined the expression levels of proteins associated with the outer membrane (OM) of the ancestor and evolved strains, whose membrane-related GO functional categories were over-represented in the evolution-specific co-expression networks (Figure 7a-f). OM protein levels revealed substantial differential expression among the ancestor and evolved strains (Figure 8). In Adp lines, GltB (glutamate synthase [nicotinamide adenine dinucleotide phosphate (NADPH)] large chain precursor), LamB (maltose high-affinity receptor), and YaeT (polypeptide involved in outer-membrane protein biogenesis) proteins were over-expressed; whereas in Stat lines FepA (outer receptor for ferric enterobactin), CirA (outer membrane receptor for iron-regulated colicin I receptor), OmpC (outer membrane porin), and OmpA (outer-membrane porin) proteins were differentially over-expressed (Figure 8). Significantly, we observed parallelism in the level of protein expression patterns in these evolved strains and involvement of the outer membrane proteins in these evolutionary processes.

Bottom Line: Excess nutrient adapted lines were found to exhibit greater degrees of positive correlation, indicating parallelism between ancestor and evolved lines, when compared with prolonged stationary phase adapted lines.Gene-metabolite correlation network analysis revealed over-representation of membrane-associated functional categories.GltB, LamB and YaeT proteins in excess nutrient lines, and FepA, CirA, OmpC and OmpA in prolonged stationary phase lines were found to be differentially over-expressed.

View Article: PubMed Central - HTML - PubMed

Affiliation: International NRW Graduate School in Bioinformatics and Genome Research, Bielefeld University, D-33594 Bielefeld, Germany. cvijayen@cebitec.uni-bielefeld.de

ABSTRACT

Background: Evolutionary changes that are due to different environmental conditions can be examined based on the various molecular aspects that constitute a cell, namely transcript, protein, or metabolite abundance. We analyzed changes in transcript and metabolite abundance in evolved and ancestor strains in three different evolutionary conditions - excess nutrient adaptation, prolonged stationary phase adaptation, and adaptation because of environmental shift - in two different strains of bacterium Escherichia coli K-12 (MG1655 and DH10B).

Results: Metabolite profiling of 84 identified metabolites revealed that most of the metabolites involved in the tricarboxylic acid cycle and nucleotide metabolism were altered in both of the excess nutrient evolved lines. Gene expression profiling using whole genome microarray with 4,288 open reading frames revealed over-representation of the transport functional category in all evolved lines. Excess nutrient adapted lines were found to exhibit greater degrees of positive correlation, indicating parallelism between ancestor and evolved lines, when compared with prolonged stationary phase adapted lines. Gene-metabolite correlation network analysis revealed over-representation of membrane-associated functional categories. Proteome analysis revealed the major role played by outer membrane proteins in adaptive evolution. GltB, LamB and YaeT proteins in excess nutrient lines, and FepA, CirA, OmpC and OmpA in prolonged stationary phase lines were found to be differentially over-expressed.

Conclusion: In summary, we report the vital involvement of energy metabolism and membrane-associated functional categories in all of the evolutionary conditions examined in this study within the context of transcript, outer membrane protein, and metabolite levels. These initial data obtained may help to enhance our understanding of the evolutionary process from a systems biology perspective.

Show MeSH
Related in: MedlinePlus