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Effect of random and hub gene disruptions on environmental and mutational robustness in Escherichia coli.

Cooper TF, Morby AP, Gunn A, Schneider D - BMC Genomics (2006)

Bottom Line: We found that disruption of random genes had less effect on robustness to environmental stress than did the targeted disruption of hub genes.When we compared the effect of each disruption on environmental and mutational stress, we found a negative relationship, such that strains that were more environmentally robust tended to be less robust to mutational stress.That E. coli can reduce the effect of environmental stress without reducing the phenotypic effect of additional mutations, indicates that robustness and evolvability need not be antagonistic.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Biological Sciences, University of Auckland, Auckland, New Zealand. t.cooper@auckland.ac.nz

ABSTRACT

Background: Genome-wide profiling has allowed the regulatory interaction networks of many organisms to be visualised and the pattern of connections between genes to be studied. These networks are non-random, following a power-law distribution with a small number of well-connected 'hubs' and many genes with only one or a few connections. Theoretical work predicts that power-law networks display several unique properties. One of the most biologically interesting of these is an intrinsic robustness to disturbance such that removal of a random gene will have little effect on network function. Conversely, targeted removal of a hub gene is expected to have a large effect.

Results: We compared the response of Escherichia coli to environmental and mutational stress following disruption of random or hub genes. We found that disruption of random genes had less effect on robustness to environmental stress than did the targeted disruption of hub genes. In contrast, random disruption strains were slightly less robust to the effect of mutational stress than were hub disruption strains. When we compared the effect of each disruption on environmental and mutational stress, we found a negative relationship, such that strains that were more environmentally robust tended to be less robust to mutational stress.

Conclusion: Our results demonstrate that mutant strains of E. coli respond differently to stress, depending on whether random or hub genes are disrupted. This difference indicates that the power-law distribution of regulatory interactions has biological significance, making random disruptions less deleterious to organisms facing environmental stress. That E. coli can reduce the effect of environmental stress without reducing the phenotypic effect of additional mutations, indicates that robustness and evolvability need not be antagonistic.

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Robustness of random and hub deletion mutants to environmental stress. Average of median values measured in each environment is plotted for each strain. Error bars indicate standard errors. Reference strain (ref), solid square, random disruption strains, solid circles; targeted hub disruption strains, hollow circles. Solid line indicates mean of random disruption strains; dotted line indicates mean of targeted hub disruption strains.
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Figure 2: Robustness of random and hub deletion mutants to environmental stress. Average of median values measured in each environment is plotted for each strain. Error bars indicate standard errors. Reference strain (ref), solid square, random disruption strains, solid circles; targeted hub disruption strains, hollow circles. Solid line indicates mean of random disruption strains; dotted line indicates mean of targeted hub disruption strains.

Mentions: To detect differences in the robustness of disruption strains to environmental stress we measured the growth rate of each strain in each of fifteen stressful environments (Materials and Methods) (figure 2). Each measurement was paired with a measurement of the same strain in the reference environment. Taking the log ratio of these measurements allowed us to normalize measurements, factoring out the specific biochemical effect of a mutation from its general effect on response to stress.


Effect of random and hub gene disruptions on environmental and mutational robustness in Escherichia coli.

Cooper TF, Morby AP, Gunn A, Schneider D - BMC Genomics (2006)

Robustness of random and hub deletion mutants to environmental stress. Average of median values measured in each environment is plotted for each strain. Error bars indicate standard errors. Reference strain (ref), solid square, random disruption strains, solid circles; targeted hub disruption strains, hollow circles. Solid line indicates mean of random disruption strains; dotted line indicates mean of targeted hub disruption strains.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1590030&req=5

Figure 2: Robustness of random and hub deletion mutants to environmental stress. Average of median values measured in each environment is plotted for each strain. Error bars indicate standard errors. Reference strain (ref), solid square, random disruption strains, solid circles; targeted hub disruption strains, hollow circles. Solid line indicates mean of random disruption strains; dotted line indicates mean of targeted hub disruption strains.
Mentions: To detect differences in the robustness of disruption strains to environmental stress we measured the growth rate of each strain in each of fifteen stressful environments (Materials and Methods) (figure 2). Each measurement was paired with a measurement of the same strain in the reference environment. Taking the log ratio of these measurements allowed us to normalize measurements, factoring out the specific biochemical effect of a mutation from its general effect on response to stress.

Bottom Line: We found that disruption of random genes had less effect on robustness to environmental stress than did the targeted disruption of hub genes.When we compared the effect of each disruption on environmental and mutational stress, we found a negative relationship, such that strains that were more environmentally robust tended to be less robust to mutational stress.That E. coli can reduce the effect of environmental stress without reducing the phenotypic effect of additional mutations, indicates that robustness and evolvability need not be antagonistic.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Biological Sciences, University of Auckland, Auckland, New Zealand. t.cooper@auckland.ac.nz

ABSTRACT

Background: Genome-wide profiling has allowed the regulatory interaction networks of many organisms to be visualised and the pattern of connections between genes to be studied. These networks are non-random, following a power-law distribution with a small number of well-connected 'hubs' and many genes with only one or a few connections. Theoretical work predicts that power-law networks display several unique properties. One of the most biologically interesting of these is an intrinsic robustness to disturbance such that removal of a random gene will have little effect on network function. Conversely, targeted removal of a hub gene is expected to have a large effect.

Results: We compared the response of Escherichia coli to environmental and mutational stress following disruption of random or hub genes. We found that disruption of random genes had less effect on robustness to environmental stress than did the targeted disruption of hub genes. In contrast, random disruption strains were slightly less robust to the effect of mutational stress than were hub disruption strains. When we compared the effect of each disruption on environmental and mutational stress, we found a negative relationship, such that strains that were more environmentally robust tended to be less robust to mutational stress.

Conclusion: Our results demonstrate that mutant strains of E. coli respond differently to stress, depending on whether random or hub genes are disrupted. This difference indicates that the power-law distribution of regulatory interactions has biological significance, making random disruptions less deleterious to organisms facing environmental stress. That E. coli can reduce the effect of environmental stress without reducing the phenotypic effect of additional mutations, indicates that robustness and evolvability need not be antagonistic.

Show MeSH
Related in: MedlinePlus