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Describing the structural robustness landscape of bacterial small RNAs.

Rodrigo G, Fares MA - BMC Evol. Biol. (2012)

Bottom Line: We found that bacterial sncRNAs are not significantly robust to both mutational and environmental perturbations when compared against artificial, unbiased sequences.We further found that, on average, epistasis in bacterial sncRNAs is significantly antagonistic, and positively correlates with plasticity.As a result, plasticity emerges to link robustness, functionality and evolvability.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas, Universidad Politécnica de Valencia, Ingeniero Fausto Elio s/n, 46022 Valencia, Spain. guirodta@ibmcp.upv.es

ABSTRACT

Background: The potential role of RNA molecules as gene expression regulators has led to a new perspective on the intracellular control and genome organization. Because secondary structures are crucial for their regulatory role, we sought to investigate their robustness to mutations and environmental changes.

Results: Here, we dissected the structural robustness landscape of the small non-coding RNAs (sncRNAs) encoded in the genome of the bacterium Escherichia coli. We found that bacterial sncRNAs are not significantly robust to both mutational and environmental perturbations when compared against artificial, unbiased sequences. However, we found that, on average, bacterial sncRNAs tend to be significantly plastic, and that mutational and environmental robustness strongly correlate. We further found that, on average, epistasis in bacterial sncRNAs is significantly antagonistic, and positively correlates with plasticity. Moreover, the evolution of robustness is likely dependent upon the environmental stability of the cell, with more fluctuating environments leading to the emergence and fixation of more robust molecules. Mutational robustness also appears to be correlated with structural functionality and complexity.

Conclusion: Our study provides a deep characterization of the structural robustness landscape of bacterial sncRNAs, suggesting that evolvability could be evolved as a consequence of selection for more plastic molecules. It also supports that environmental fluctuations could promote mutational robustness. As a result, plasticity emerges to link robustness, functionality and evolvability.

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Correlation between mutational and environmental robustness. Computation of mutational and environmental robustness (Rm and Re) for different sncRNAs and their corresponding structural analogs. The robustness of artificial sequences sharing the natural structure was evaluated (γ gives the value of the slope). Solid lines indicate the values for the natural sequence.
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Figure 5: Correlation between mutational and environmental robustness. Computation of mutational and environmental robustness (Rm and Re) for different sncRNAs and their corresponding structural analogs. The robustness of artificial sequences sharing the natural structure was evaluated (γ gives the value of the slope). Solid lines indicate the values for the natural sequence.

Mentions: We further dissected and quantified robustness in the different sncRNA molecules. Interestingly, not all sncRNAs displayed the same level of robustness: a fraction of sncRNAs has not evolved to greater robustness (e.g., C0664), while the majority of them have reached suboptimal levels of robustness (e.g., dsrA) (Figures 5 and S6). The most robust gene was micF, to both mutations (z = 2.05) and environmental changes (z = 2.34), whereas the less robust gene was C0064, to both mutations (z = -5.87) and environmental changes (z = -5.82). MicF is a stress response sncRNA that targets the membrane protein OmpF and other genes related to chemotaxis [32,33]. However, its structure is very simple, with most of the nucleotides remaining unpaired, hence perturbations have minimal effects on the stability of this gene. On the contrary, C0064 is an enzyme with transferase activity that modifies rRNA and has been identified as the most plastic of the bacterial sncRNAs (z = 7.33). Environmental robustness strongly correlates with mutational robustness so that the promotion of one variable entails a proportional effect on the other (Figures 4, 5, and S7). Of relevance is the fact that the variability in sequence compositions that share a common structure was considerable and allowed unraveling a precise pattern by which the more robust molecules to environmental perturbations were also those more robust to mutational perturbations. This reinforces the fact that these two variables are not independent; hence the congruent evolution of the two robustness variables [11,12] in the case of bacterial sncRNAs becomes a plausible hypothesis.


Describing the structural robustness landscape of bacterial small RNAs.

Rodrigo G, Fares MA - BMC Evol. Biol. (2012)

Correlation between mutational and environmental robustness. Computation of mutational and environmental robustness (Rm and Re) for different sncRNAs and their corresponding structural analogs. The robustness of artificial sequences sharing the natural structure was evaluated (γ gives the value of the slope). Solid lines indicate the values for the natural sequence.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3368786&req=5

Figure 5: Correlation between mutational and environmental robustness. Computation of mutational and environmental robustness (Rm and Re) for different sncRNAs and their corresponding structural analogs. The robustness of artificial sequences sharing the natural structure was evaluated (γ gives the value of the slope). Solid lines indicate the values for the natural sequence.
Mentions: We further dissected and quantified robustness in the different sncRNA molecules. Interestingly, not all sncRNAs displayed the same level of robustness: a fraction of sncRNAs has not evolved to greater robustness (e.g., C0664), while the majority of them have reached suboptimal levels of robustness (e.g., dsrA) (Figures 5 and S6). The most robust gene was micF, to both mutations (z = 2.05) and environmental changes (z = 2.34), whereas the less robust gene was C0064, to both mutations (z = -5.87) and environmental changes (z = -5.82). MicF is a stress response sncRNA that targets the membrane protein OmpF and other genes related to chemotaxis [32,33]. However, its structure is very simple, with most of the nucleotides remaining unpaired, hence perturbations have minimal effects on the stability of this gene. On the contrary, C0064 is an enzyme with transferase activity that modifies rRNA and has been identified as the most plastic of the bacterial sncRNAs (z = 7.33). Environmental robustness strongly correlates with mutational robustness so that the promotion of one variable entails a proportional effect on the other (Figures 4, 5, and S7). Of relevance is the fact that the variability in sequence compositions that share a common structure was considerable and allowed unraveling a precise pattern by which the more robust molecules to environmental perturbations were also those more robust to mutational perturbations. This reinforces the fact that these two variables are not independent; hence the congruent evolution of the two robustness variables [11,12] in the case of bacterial sncRNAs becomes a plausible hypothesis.

Bottom Line: We found that bacterial sncRNAs are not significantly robust to both mutational and environmental perturbations when compared against artificial, unbiased sequences.We further found that, on average, epistasis in bacterial sncRNAs is significantly antagonistic, and positively correlates with plasticity.As a result, plasticity emerges to link robustness, functionality and evolvability.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas, Universidad Politécnica de Valencia, Ingeniero Fausto Elio s/n, 46022 Valencia, Spain. guirodta@ibmcp.upv.es

ABSTRACT

Background: The potential role of RNA molecules as gene expression regulators has led to a new perspective on the intracellular control and genome organization. Because secondary structures are crucial for their regulatory role, we sought to investigate their robustness to mutations and environmental changes.

Results: Here, we dissected the structural robustness landscape of the small non-coding RNAs (sncRNAs) encoded in the genome of the bacterium Escherichia coli. We found that bacterial sncRNAs are not significantly robust to both mutational and environmental perturbations when compared against artificial, unbiased sequences. However, we found that, on average, bacterial sncRNAs tend to be significantly plastic, and that mutational and environmental robustness strongly correlate. We further found that, on average, epistasis in bacterial sncRNAs is significantly antagonistic, and positively correlates with plasticity. Moreover, the evolution of robustness is likely dependent upon the environmental stability of the cell, with more fluctuating environments leading to the emergence and fixation of more robust molecules. Mutational robustness also appears to be correlated with structural functionality and complexity.

Conclusion: Our study provides a deep characterization of the structural robustness landscape of bacterial sncRNAs, suggesting that evolvability could be evolved as a consequence of selection for more plastic molecules. It also supports that environmental fluctuations could promote mutational robustness. As a result, plasticity emerges to link robustness, functionality and evolvability.

Show MeSH
Related in: MedlinePlus