Evolving metabolism of 2,4-dinitrotoluene triggers SOS-independent diversification of host cells

Environmental Microbiology

Volumn 21, Issue 1, 2019, Pages 314-326

  Akkaya, Özlem ^a,b   Nikel, Pablo I ^c   Pérez Pantoja, Danilo ^d   de Lorenzo, Víctor ^b  

^a GEBZE TECHNICAL UNIVERSITY   (Turkey)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c Chalmers University of Technology   (Denmark)

^d UNIVERSIDAD TECNOLÓGICA METROPOLITANA   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

2,4-DINITROTOLUENE; BACTERIAL PROTEIN; DNA BINDING PROTEIN; DNA DIRECTED RNA POLYMERASE; ESCHERICHIA COLI PROTEIN; NITROBENZENE DERIVATIVE; REACTIVE OXYGEN METABOLITE; RECA PROTEIN; RECA PROTEIN, E COLI; RPOB PROTEIN, E COLI; SIGMA FACTOR; SIGMA FACTOR KATF PROTEIN, BACTERIA;

BIOREMEDIATION; BURKHOLDERIA CEPACIA; DNA DAMAGE; DNA REPLICATION; ESCHERICHIA COLI; GENETICS; METABOLISM; MUTAGENESIS; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHYSIOLOGY;

BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; BURKHOLDERIA CEPACIA; DINITROBENZENES; DNA DAMAGE; DNA REPLICATION; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; METABOLIC NETWORKS AND PATHWAYS; MUTAGENESIS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REC A RECOMBINASES; SIGMA FACTOR; SOS RESPONSE, GENETICS;

EID: 85058048537     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.14459     Document Type: Article

References (48)

1. Akkaya, O., Pérez-Pantoja, D., Calles, B., Nikel, P. I., and de Lorenzo, V. (2018) The metabolic redox regime of Pseudomonas putida tunes its evolvability towards novel xenobiotic substrates. mBio 9: e01512–18; https://doi.org/10.1128/mBio.01512-18.
2. Andersson, D. I., and Hughes, D. (2014) Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol 12: 465–478.
3. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Sys Biol 2: 0008.
4. Becerra, M. C., Eraso, A. J., and Albesa, I. (2003) Comparison of oxidative stress induced by ciprofloxacin and pyoverdin in bacteria and in leukocytes to evaluate toxicity. Luminescence 18: 334–340.
5. Benedetti, I. M., de Lorenzo, V., and Silva-Rocha, R. (2012) Quantitative, non-disruptive monitoring of transcription in single cells with a broad-host range GFP-luxCDABE dual reporter system. PLoS One 7: e52000.
6. Blattner, F. R., Plunkett, G., III, Bloch, C. A., Perna, N. T., Burland, V., Riley, M., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453–1462.
7. Blazquez, J., Rodrıguez-Beltran, J., and Matic, I. (2018) Antibiotic-induced genetic variation: how it arises and how it can be prevented. Ann Rev Microbiol 72: 209–230.
8. Bolin, C., and Cardozo-Pelaez, F. (2007) Assessing biomarkers of oxidative stress: analysis of guanosine and oxidized guanosine nucleotide triphosphates by high performance liquid chromatography with electrochemical detection. J Chrom B 856: 121–130.
9. Chen, J., and Gottesman, S. (2017) Hfq links translation repression to stress-induced mutagenesis in E. coli. Genes Dev 31: 1382–1395.
10. Dapa, T., Fleurier, S., Bredeche, M. F., and Matic, I. (2017) The SOS and RpoS regulons contribute to bacterial cell robustness to genotoxic stress by synergistically regulating DNA polymerase pol II. Genetics 206: 1349–1360.
11. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640–6645.
12. de Las Heras, A., Chavarria, M., and de Lorenzo, V. (2011) Association of dnt genes of Burkholderia sp. DNT with the substrate-blind regulator DntR draws the evolutionary itinerary of 2,4-dinitrotoluene biodegradation. Mol Microbiol 82: 287–299.
13. Elez, M., Radman, M., and Matic, I. (2007) The frequency and structure of recombinant products is determined by the cellular level of MutL. Proc Natl Acad Sci U S A 104: 8935–8940.
14. Foster, P. L. (2005) Stress responses and genetic variation in bacteria. Mutat Res 569: 3–11.
15. Galhardo, R. S., Do, R., Yamada, M., Friedberg, E. C., Hastings, P. J., Nohmi, T., and Rosenberg, S. M. (2009) DinB upregulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. Genetics 182: 55–68.
16. Gullberg, E., Cao, S., Berg, O. G., Ilback, C., Sandegren, L., Hughes, D., and Andersson, D. I. (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7: e1002158.
17. Gutierrez, A., Laureti, L., Crussard, S., Abida, H., Rodriguez-Rojas, A., Blazquez, J., et al. (2013) Beta-lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun 4: 1610.
18. Hanahan, D., and Meselson, M. (1983) Plasmid screening at high colony density. Methods Enzymol 100: 333–342.
19. Hastings, P. J., Hersh, M. N., Thornton, P. C., Fonville, N. C., Slack, A., Frisch, R. L., et al. (2010) Competition of Escherichia coli DNA polymerases I, II and III with DNA pol IV in stressed cells. PLoS One 5: e10862.
20. Herrero, M., de Lorenzo, V., and Timmis, K. N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557–6567.
21. Ilmjarv, T., Naanuri, E., and Kivisaar, M. (2017) Contribution of increased mutagenesis to the evolution of pollutants-degrading indigenous bacteria. PLoS One 12: e0182484.
22. Johnson, G. R., and Spain, J. C. (2003) Evolution of catabolic pathways for synthetic compounds: bacterial pathways for degradation of 2,4-dinitrotoluene and nitrobenzene. Appl Microbiol Biotechnol 62: 110–123.
23. Johnson, G. R., Jain, R. K., and Spain, J. C. (2002) Origins of the 2,4-dinitrotoluene pathway. J Bacteriol 184: 4219–4232.
24. Ju, K. S., and Parales, R. E. (2010) Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74: 250–272.
25. Kalapila, A. G., Loktionova, N. A., and Pegg, A. E. (2008) Alkyltransferase-mediated toxicity of 1,3-butadiene diepoxide. Chem Res Toxicol 21: 1851–1861.
26. Kessinger, T. A., and Van Cleve, J. (2018) Genetic draft and valley crossing. bioRxiv. https://doi.org/10.1101/383737.
27. Kohanski, M. A., DePristo, M. A., and Collins, J. J. (2010) Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol Cell 37: 311–320.
28. Kovacic, P., and Somanathan, R. (2014) Nitroaromatic compounds: environmental toxicity, carcinogenicity, mutagenicity, therapy and mechanism. J Appl Toxicol 34: 810–824.
29. Krisko, A., and Radman, M. (2013) Phenotypic and genetic consequences of protein damage. PLoS Genet 9: e1003810.
30. Layton, J. C., and Foster, P. L. (2003) Error-prone DNA polymerase IV is controlled by the stress-response sigma factor, RpoS, in Escherichia coli. Mol Microbiol 50: 549–561.
31. Li, G.-M. (2008) Mechanisms and functions of DNA mismatch repair. Cell Res 18: 85–98.
32. Lopez, E., and Blazquez, J. (2009) Effect of subinhibitory concentrations of antibiotics on intrachromosomal homologous recombination in Escherichia coli. Antimicrob Agents Chemother 53: 3411–3415.
33. Lopez, E., Elez, M., Matic, I., and Blazquez, J. (2007) Antibiotic-mediated recombination: ciprofloxacin stimulates SOS-independent recombination of divergent sequences in Escherichia coli. Mol Microbiol 64: 83–93.
34. Martinez-Garcia, E., Aparicio, T., de Lorenzo, V., and Nikel, P. I. (2014) New transposon tools tailored for metabolic engineering of Gram-negative microbial cell factories. Front Bioeng Biotechnol 2: 46.
35. Michel, B. (2005) After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol 3: e255.
36. Nikel, P. I., Perez-Pantoja, D., and de Lorenzo, V. (2013) Why are chlorinated pollutants so difficult to degrade aerobically? Redox stress limits 1,3-dichloroprop-1-ene metabolism by Pseudomonas pavonaceae. Philos Trans R Soc Lond B Biol Sci 368: 20120377.
37. Nishino, S. F., Paoli, G. C., and Spain, J. C. (2000) Aerobic degradation of dinitrotoluenes and pathway for bacterial degradation of 2,6-dinitrotoluene. Appl Environ Microbiol 66: 2139–2147.
38. Perez-Pantoja, D., Nikel, P. I., Chavarria, M., and de Lorenzo, V. (2013) Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria. PLoS Genet 9: e1003764.
39. Phillips, I., Culebras, E., Moreno, F., and Baquero, F. (1987) Induction of the SOS response by new 4-quinolones. J Antimicrob Chemother 20: 631–638.
40. Piddock, L. J. V., and Wise, R. (1987) Induction of the SOS response in Escherichia coli by 4-quinolone antimicrobial agents. FEMS Microbiol Lett 41: 289–294.
41. Rosche, W. A., and Foster, P. L. (2000) Determining mutation rates in bacterial populations. Methods 20: 4–17.
42. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory Press.
43. Sikkema, J., de Bont, J. A., and Poolman, B. (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59: 201–222.
44. Silva-Rocha, R., Martinez-Garcia, E., Calles, B., Chavarria, M., Arce-Rodriguez, A., de Las Heras, A., et al. (2013) The standard European vector architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res 41: D666–D675.
45. Spanggord, R. J., Spain, J. C., Nishino, S. F., and Mortelmans, K. E. (1991) Biodegradation of 2,4-dinitrotoluene by a pseudomonas sp. Appl Environ Microbiol 57: 3200–3205.
46. Suen, W. C., Haigler, B. E., and Spain, J. C. (1996) 2,4-Dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: similarity to naphthalene dioxygenase. J Bacteriol 178: 4926–4934.
47. Tenaillon, O., Denamur, E., and Matic, I. (2004) Evolutionary significance of stress-induced mutagenesis in bacteria. Trends Microbiol 12: 264–270.
48. Veaute, X., Delmas, S., Selva, M., Jeusset, J., Le Cam, E., Matic, I., et al. (2005) UvrD helicase, unlike rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J 24: 180–189.