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Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria.

Pérez-Pantoja D, Nikel PI, Chavarría M, de Lorenzo V - PLoS Genet. (2013)

Bottom Line: DNT mineralizes the xenobiotic compound 2,4-dinitrotoluene (DNT) owing to the catabolic dnt genes borne by plasmid DNT, but the process fails to promote significant growth.Naphthalene, the ancestral substrate of the dioxygenase from which DntA has evolved, also caused significant ROS formation.It is thus plausible that the evolutionary roadmap for biodegradation of xenobiotic compounds like DNT was largely elicited by mutagenic oxidative stress caused by faulty reactions of precursor enzymes with novel but structurally related substrates-to-be.

View Article: PubMed Central - PubMed

Affiliation: Systems and Synthetic Biology Program, Centro Nacional de Biotecnología, CSIC, Campus de Cantoblanco, Madrid, Spain.

ABSTRACT
Environmental strain Burkholderia sp. DNT mineralizes the xenobiotic compound 2,4-dinitrotoluene (DNT) owing to the catabolic dnt genes borne by plasmid DNT, but the process fails to promote significant growth. To investigate this lack of physiological return of such an otherwise complete metabolic route, cells were exposed to DNT under various growth conditions and the endogenous formation of reactive oxygen species (ROS) monitored in single bacteria. These tests revealed the buildup of a strong oxidative stress in the population exposed to DNT. By either curing the DNT plasmid or by overproducing the second activity of the biodegradation route (DntB) we could trace a large share of ROS production to the first reaction of the route, which is executed by the multicomponent dioxygenase encoded by the dntA gene cluster. Naphthalene, the ancestral substrate of the dioxygenase from which DntA has evolved, also caused significant ROS formation. That both the old and the new substrate brought about a considerable cellular stress was indicative of a still-evolving DntA enzyme which is neither optimal any longer for naphthalene nor entirely advantageous yet for growth of the host strain on DNT. We could associate endogenous production of ROS with likely error-prone repair mechanisms of DNA damage, and the ensuing stress-induced mutagenesis in cells exposed to DNT. It is thus plausible that the evolutionary roadmap for biodegradation of xenobiotic compounds like DNT was largely elicited by mutagenic oxidative stress caused by faulty reactions of precursor enzymes with novel but structurally related substrates-to-be.

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Antifragility governs evolution of new pathways for xenobiotic compounds.The cartoon sketches the differences between fragile (collapse after a shock), robust (recovery to the same state of affairs after a shock) and anti-fragile (improvement after a shock) systems. In the case examined in this study, we argue that the ROS produced by faulty dioxygenation reactions produces a considerable chemical insult which on one hand places the population at the verge of collapse (>70% mortality, see Fig. 2) but simultaneously diversifies genetically the same population and thus fosters the exploration of the solution space. The term antifragility was originally coined for Economics [55] but has been recently applied to biological systems as well [54]. The concept is reminiscent (but not entirely equivalent) to hormesis[67] in that the post-challenge strength goes beyond a superior tolerance to the original insult, and therefore results in a general adaptive phenotype.
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pgen-1003764-g009: Antifragility governs evolution of new pathways for xenobiotic compounds.The cartoon sketches the differences between fragile (collapse after a shock), robust (recovery to the same state of affairs after a shock) and anti-fragile (improvement after a shock) systems. In the case examined in this study, we argue that the ROS produced by faulty dioxygenation reactions produces a considerable chemical insult which on one hand places the population at the verge of collapse (>70% mortality, see Fig. 2) but simultaneously diversifies genetically the same population and thus fosters the exploration of the solution space. The term antifragility was originally coined for Economics [55] but has been recently applied to biological systems as well [54]. The concept is reminiscent (but not entirely equivalent) to hormesis[67] in that the post-challenge strength goes beyond a superior tolerance to the original insult, and therefore results in a general adaptive phenotype.

Mentions: In sum, the data above strongly argue that evolution of DNT biodegradation pathways and possibly of many other catabolic systems, ultimately benefit from the mutagenic stress caused by faulty reactions of pre-existing enzymes on suboptimal substrates. The term anti-fragility (as opposed to robustness, [54], [55]) has been recently coined for describing such systems that reach a higher peak of efficacy after having nearly collapsed with stress and shocks (Fig. 9). The results discussed in this work seem not only to place the appearance of new xenobiotic-biodegradation strains within such an evolutionary scenario, but also suggest experimental approaches to accelerate their emergence in the Laboratory.


Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria.

Pérez-Pantoja D, Nikel PI, Chavarría M, de Lorenzo V - PLoS Genet. (2013)

Antifragility governs evolution of new pathways for xenobiotic compounds.The cartoon sketches the differences between fragile (collapse after a shock), robust (recovery to the same state of affairs after a shock) and anti-fragile (improvement after a shock) systems. In the case examined in this study, we argue that the ROS produced by faulty dioxygenation reactions produces a considerable chemical insult which on one hand places the population at the verge of collapse (>70% mortality, see Fig. 2) but simultaneously diversifies genetically the same population and thus fosters the exploration of the solution space. The term antifragility was originally coined for Economics [55] but has been recently applied to biological systems as well [54]. The concept is reminiscent (but not entirely equivalent) to hormesis[67] in that the post-challenge strength goes beyond a superior tolerance to the original insult, and therefore results in a general adaptive phenotype.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3757077&req=5

pgen-1003764-g009: Antifragility governs evolution of new pathways for xenobiotic compounds.The cartoon sketches the differences between fragile (collapse after a shock), robust (recovery to the same state of affairs after a shock) and anti-fragile (improvement after a shock) systems. In the case examined in this study, we argue that the ROS produced by faulty dioxygenation reactions produces a considerable chemical insult which on one hand places the population at the verge of collapse (>70% mortality, see Fig. 2) but simultaneously diversifies genetically the same population and thus fosters the exploration of the solution space. The term antifragility was originally coined for Economics [55] but has been recently applied to biological systems as well [54]. The concept is reminiscent (but not entirely equivalent) to hormesis[67] in that the post-challenge strength goes beyond a superior tolerance to the original insult, and therefore results in a general adaptive phenotype.
Mentions: In sum, the data above strongly argue that evolution of DNT biodegradation pathways and possibly of many other catabolic systems, ultimately benefit from the mutagenic stress caused by faulty reactions of pre-existing enzymes on suboptimal substrates. The term anti-fragility (as opposed to robustness, [54], [55]) has been recently coined for describing such systems that reach a higher peak of efficacy after having nearly collapsed with stress and shocks (Fig. 9). The results discussed in this work seem not only to place the appearance of new xenobiotic-biodegradation strains within such an evolutionary scenario, but also suggest experimental approaches to accelerate their emergence in the Laboratory.

Bottom Line: DNT mineralizes the xenobiotic compound 2,4-dinitrotoluene (DNT) owing to the catabolic dnt genes borne by plasmid DNT, but the process fails to promote significant growth.Naphthalene, the ancestral substrate of the dioxygenase from which DntA has evolved, also caused significant ROS formation.It is thus plausible that the evolutionary roadmap for biodegradation of xenobiotic compounds like DNT was largely elicited by mutagenic oxidative stress caused by faulty reactions of precursor enzymes with novel but structurally related substrates-to-be.

View Article: PubMed Central - PubMed

Affiliation: Systems and Synthetic Biology Program, Centro Nacional de Biotecnología, CSIC, Campus de Cantoblanco, Madrid, Spain.

ABSTRACT
Environmental strain Burkholderia sp. DNT mineralizes the xenobiotic compound 2,4-dinitrotoluene (DNT) owing to the catabolic dnt genes borne by plasmid DNT, but the process fails to promote significant growth. To investigate this lack of physiological return of such an otherwise complete metabolic route, cells were exposed to DNT under various growth conditions and the endogenous formation of reactive oxygen species (ROS) monitored in single bacteria. These tests revealed the buildup of a strong oxidative stress in the population exposed to DNT. By either curing the DNT plasmid or by overproducing the second activity of the biodegradation route (DntB) we could trace a large share of ROS production to the first reaction of the route, which is executed by the multicomponent dioxygenase encoded by the dntA gene cluster. Naphthalene, the ancestral substrate of the dioxygenase from which DntA has evolved, also caused significant ROS formation. That both the old and the new substrate brought about a considerable cellular stress was indicative of a still-evolving DntA enzyme which is neither optimal any longer for naphthalene nor entirely advantageous yet for growth of the host strain on DNT. We could associate endogenous production of ROS with likely error-prone repair mechanisms of DNA damage, and the ensuing stress-induced mutagenesis in cells exposed to DNT. It is thus plausible that the evolutionary roadmap for biodegradation of xenobiotic compounds like DNT was largely elicited by mutagenic oxidative stress caused by faulty reactions of precursor enzymes with novel but structurally related substrates-to-be.

Show MeSH
Related in: MedlinePlus