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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.

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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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Distributions of structural properties for tRNAs. Histograms of plasticity (P), mutational and environmental robustness (Rm and Re) for the bacterial tRNAs.
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Figure 7: Distributions of structural properties for tRNAs. Histograms of plasticity (P), mutational and environmental robustness (Rm and Re) for the bacterial tRNAs.

Mentions: To further investigate the relationship between RNA function and robustness, we calculated P, Rm and Re for the bacterial tRNAs (Figure 7) (sequences from GtRNAdb [39]). Because those tRNAs have a length between 74 and 93 nucleotides, we compared them against the sncRNAs with L < 100, although similar results were obtained for the whole set of sncRNAs. We observed that sncRNAs are significantly more robust, both to mutations and environmental perturbations, than tRNAs (U-test, P-value < 10-8 for Rm and Re), and significantly less plastic (U-test, P-value = 0.01, although the distributions are not normal). This could in principle indicate that the higher conservation of tRNAs is a consequence of low structural robustness, where one mutation would have a more severe effect than over a given sncRNA. This comparison points out differences in robustness of two RNA functional groups. However, the function of an RNA molecule is usually associated to the expression of one or various proteins. In particular, Hfq is an RNA chaperone that binds to sncRNAs for stabilization and assisting the interaction with the target mRNA [40]. We also know that tRNAs present great stability because they are recognized by endogenous enzymes that prevent degradation by nucleases, which allow tRNAs to accumulate in high concentrations within the cell [41]. Hence, it would be indebted to account for those endogenous enzymes to further link RNA robustness and functionality, for example by looking at mutations in the RNA sequence falling down in the protein recognition site.


Describing the structural robustness landscape of bacterial small RNAs.

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

Distributions of structural properties for tRNAs. Histograms of plasticity (P), mutational and environmental robustness (Rm and Re) for the bacterial tRNAs.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Distributions of structural properties for tRNAs. Histograms of plasticity (P), mutational and environmental robustness (Rm and Re) for the bacterial tRNAs.
Mentions: To further investigate the relationship between RNA function and robustness, we calculated P, Rm and Re for the bacterial tRNAs (Figure 7) (sequences from GtRNAdb [39]). Because those tRNAs have a length between 74 and 93 nucleotides, we compared them against the sncRNAs with L < 100, although similar results were obtained for the whole set of sncRNAs. We observed that sncRNAs are significantly more robust, both to mutations and environmental perturbations, than tRNAs (U-test, P-value < 10-8 for Rm and Re), and significantly less plastic (U-test, P-value = 0.01, although the distributions are not normal). This could in principle indicate that the higher conservation of tRNAs is a consequence of low structural robustness, where one mutation would have a more severe effect than over a given sncRNA. This comparison points out differences in robustness of two RNA functional groups. However, the function of an RNA molecule is usually associated to the expression of one or various proteins. In particular, Hfq is an RNA chaperone that binds to sncRNAs for stabilization and assisting the interaction with the target mRNA [40]. We also know that tRNAs present great stability because they are recognized by endogenous enzymes that prevent degradation by nucleases, which allow tRNAs to accumulate in high concentrations within the cell [41]. Hence, it would be indebted to account for those endogenous enzymes to further link RNA robustness and functionality, for example by looking at mutations in the RNA sequence falling down in the protein recognition site.

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