The metabolic redox regime of Pseudomonas putida tunes its evolvability toward novel xenobiotic substrates

mBio

Volumn 9, Issue 4, 2018, Pages

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

^a GEBZE TECHNICAL UNIVERSITY   (Turkey)

^b UNIVERSIDAD TECNOLÓGICA METROPOLITANA   (Chile)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^d Chalmers University of Technology   (Denmark)

Author keywords

Biodegradation; Dinitrotoluene; Evolution; NADPH oxidases; Oxidative stress; Pseudomonas putida; Reactive oxygen species

Indexed keywords

AROMATIC NITRO COMPOUND; REACTIVE OXYGEN METABOLITE; XENOBIOTIC AGENT; 2,4-DINITROTOLUENE; BACTERIAL PROTEIN; NITROBENZENE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIODEGRADATION; BURKHOLDERIA; CONTROLLED STUDY; DNA DAMAGE; GENE INSERTION; GENE MUTATION; GENETIC CODE; GENETIC COMPLEMENTATION; GENETIC STABILITY; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; OPEN READING FRAME; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS PUTIDA; BIOREMEDIATION; GENETICS; METABOLISM; MUTAGENESIS;

BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; BURKHOLDERIA; DINITROBENZENES; EVOLUTION, MOLECULAR; METABOLIC NETWORKS AND PATHWAYS; MUTAGENESIS; NADPH OXIDASES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PSEUDOMONAS PUTIDA; REACTIVE OXYGEN SPECIES; XENOBIOTICS;

EID: 85055461090     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01512-18     Document Type: Article

References (110)

1. Copley SD. 2009. Evolution of efficient pathways for degradation of anthropogenic chemicals. Nat Chem Biol 5:559–566. https://doi.org/10.1038/nchembio.197.
2. Wackett LP. 2004. Evolution of enzymes for the metabolism of new chemical inputs into the environment. J Biol Chem 279:41259–41262. https://doi.org/10.1074/jbc.R400014200.
3. Furusawa C, Horinouchi T, Maeda T. 2018. Toward prediction and control of antibiotic-resistance evolution. Curr Opin Biotechnol 54:45–49. https://doi.org/10.1016/j.copbio.2018.01.026.
4. Durão P, Balbontín R, Gordo I. 2018. Evolutionary mechanisms shaping the maintenance of antibiotic resistance. Trends Microbiol 26:677–691. https://doi.org/10.1016/j.tim.2018.01.005.
5. Palmer AC, Kishony R. 2013. Understanding, predicting and manipulating the genotypic evolution of antibiotic resistance. Nat Rev Genet 14:243–248. https://doi.org/10.1038/nrg3351.
6. Baquero F, Martínez JL. 2017. Interventions on metabolism: making antibiotic-susceptible bacteria. mBio 8:e01950-17. https://doi.org/10.1128/mBio.01950-17.
7. Seffernick JL, Wackett LP. 2016. Ancient evolution and recent evolution converge for the biodegradation of cyanuric acid and related triazines. Appl Environ Microbiol 82:1638–1645. https://doi.org/10.1128/AEM.03594-15.
8. Nishino SF, Paoli GC, Spain JC. 2000. Aerobic degradation of dinitro-toluenes and pathway for bacterial degradation of 2,6-dinitrotoluene. Appl Environ Microbiol 66:2139–2147. https://doi.org/10.1128/aem.66.5.2139-2147.2000.
9. Spain JC. 1995. Biodegradation of nitroaromatic compounds. Annu Rev Microbiol 49:523–555. https://doi.org/10.1146/annurev.mi.49.100 195.002515.
10. Kurt Z, Minoia M, Spain JC. 2018. Resveratrol as a growth substrate for bacteria from the rhizosphere. Appl Environ Microbiol 84:e00104-18. https://doi.org/10.1128/AEM.00104-18.
11. Nikel PI, Pérez-Pantoja D, 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. https://doi.org/10.1098/rstb.2012.0377.
12. van der Meer JR. 1997. Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds. Antonie Van Leeuwenhoek 71:159–178. https://doi.org/10.1023/A:1000166400935.
13. Kivisaar M. 2011. Evolution of catabolic pathways and their regulatory systems in synthetic nitroaromatic compounds degrading bacteria. Mol Microbiol 82:265–268. https://doi.org/10.1111/j.1365-2958.2011.07824.x.
14. Johnson GR, Spain JC. 2003. Evolution of catabolic pathways for synthetic compounds: bacterial pathways for degradation of 2,4-dinitrotoluene and nitrobenzene. Appl Microbiol Biotechnol 62: 110–123. https://doi.org/10.1007/s00253-003-1341-4.
15. Pérez-Pantoja D, Donoso R, Junca H, González B, Pieper DH. 2017. Phylogenomics of aerobic bacterial degradation of aromatics, p 1–48. In Rojo F (ed), Aerobic utilization of hydrocarbons, oils and lipids. Springer, Cambridge, England.
16. Pérez-Pantoja D, Donoso R, Agulló L, Córdova M, Seeger M, Pieper DH, González B. 2012. Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol 14: 1091–1117. https://doi.org/10.1111/j.1462-2920.2011.02613.x.
17. Nikel PI, Martínez-García E, de Lorenzo V. 2014. Biotechnological domestication of pseudomonads using synthetic biology. Nat Rev Microbiol 12:368–379. https://doi.org/10.1038/nrmicro3253.
18. Nikel PI, Silva-Rocha R, Benedetti I, de Lorenzo V. 2014. The private life of environmental bacteria: pollutant biodegradation at the single cell level. Environ Microbiol 16:628–642. https://doi.org/10.1111/1462-2920.12360.
19. Belda E, van Heck RGA, José Lopez-Sanchez MJ, Cruveiller S, Barbe V, Fraser C, Klenk HP, Petersen J, Morgat A, Nikel PI, Vallenet D, Rouy Z, Sekowska A, Martins dos Santos VAP, de Lorenzo V, Danchin A, Mé-digue C. 2016. The revisited genome of Pseudomonas putida KT2440 enlightens its value as a robust metabolic chassis. Environ Microbiol 18:3403–3424. https://doi.org/10.1111/1462-2920.13230.
20. Dvořák P, Nikel PI, Damborský J, de Lorenzo V. 2017. Bioremediation 3.0: engineering pollutant-removing bacteria in the times of systemic biology. Biotechnol Adv 35:845–866. https://doi.org/10.1016/j.biotechadv.2017.08.001.
21. Ju KS, Parales RE. 2010. Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74:250–272. https://doi.org/10.1128/MMBR.00006-10.
22. Parales RE, Resnick SM. 2004. Aromatic hydrocarbon dioxygenases, p 175–195. In Singh A, Ward OP (ed), Biodegradation and bioremediation, vol 2. Springer, Berlin, Germany.
23. Gibson DT, Parales RE. 2000. Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243. https://doi.org/10.1016/S0958-1669(00)00090-2.
24. Gómez-Gil L, Kumar P, Barriault D, Bolin JT, Sylvestre M, Eltis LD. 2007. Characterization of biphenyl dioxygenase of Pandoraea pnomenusa B-356 as a potent polychlorinated biphenyl-degrading enzyme. J Bacteriol 189:5705–5715. https://doi.org/10.1128/JB.01476-06.
25. Imbeault NYR, Powlowski JB, Colbert CL, Bolin JT, Eltis LD. 2000. Steady-state kinetic characterization and crystallization of a polychlorinated biphenyl-transforming dioxygenase. J Biol Chem 275:12430–12437. https://doi.org/10.1074/jbc.275.17.12430.
26. Lee K. 1999. Benzene-induced uncoupling of naphthalene dioxygenase activity and enzyme inactivation by production of hydrogen peroxide. J Bacteriol 181:2719–2725.
27. Patrauchan MA, Florizone C, Eapen S, Gómez-Gil L, Sethuraman B, Fukuda M, Davies J, Mohn WW, Eltis LD. 2008. Roles of ring-hydro-xylating dioxygenases in styrene and benzene catabolism in Rhodococcus jostii RHA1. J Bacteriol 190:37–47. https://doi.org/10.1128/JB.01122-07.
28. Parales RE, Emig MD, Lynch NA, Gibson DT. 1998. Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems. J Bacteriol 180:2337–2344.
29. Pérez-Pantoja D, González B, Pieper DH. 2010. Aerobic degradation of aromatic hydrocarbons, p 799–837. In Timmis KN (ed), Handbook of hydrocarbon and lipid microbiology, vol 2. Springer, Berlin, Germany.
30. Winkler JR, Gray HB. 2015. Electron flow through biological molecules: does hole hopping protect proteins from oxidative damage? Q Rev Biophys 48:411–420. https://doi.org/10.1017/S0033583515000062.
31. Galhardo RS, Hastings PJ, Rosenberg SM. 2007. Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 42:399–435. https://doi.org/10.1080/10409230701648502.
32. Ilmjärv T, Naanuri E, Kivisaar M. 2017. Contribution of increased mutagenesis to the evolution of pollutants-degrading indigenous bacteria. PLoS One 12:e0182484. https://doi.org/10.1371/journal.pone.0182484.
33. Spanggord RJ, Spain JC, Nishino SF, Mortelmans KE. 1991. Biodegradation of 2,4-dinitrotoluene by a Pseudomonas sp. Appl Environ Microbiol 57:3200–3205.
34. Johnson GR, Jain RK, Spain JC. 2002. Origins of the 2,4-dinitrotoluene pathway. J Bacteriol 184:4219–4232. https://doi.org/10.1128/jb.184.15.4219-4232.2002.
35. Pérez-Pantoja D, Nikel PI, Chavarría M, de Lorenzo V. 2013. Endogenous stress caused by faulty oxidation reactions fosters evolution of 2,4-dinitrotoluene-degrading bacteria. PLoS Genet 9:e1003764. https://doi.org/10.1371/journal.pgen.1003764.
36. Chen J, Gottesman S. 2017. Hfq links translation repression to stress-induced mutagenesis in E. coli. Genes Dev 31:1382–1395. https://doi.org/10.1101/gad.302547.117.
37. Gutiérrez A, Laureti L, Crussard S, Abida H, Rodríguez-Rojas A, Blázquez J, Baharoglu Z, Mazel D, Darfeuille F, Vogel J, Matic I. 2013. σ-lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun 4:1610. https://doi.org/10.1038/ncomms2607.
38. Kivisaar M. 2010. Mechanisms of stationary-phase mutagenesis in bacteria: mutational processes in pseudomonads. FEMS Microbiol Lett 312:1–14. https://doi.org/10.1111/j.1574-6968.2010.02027.x.
39. Kim J, Park W. 2014. Oxidative stress response in Pseudomonas putida. Appl Microbiol Biotechnol 98:6933–6946. https://doi.org/10.1007/s00253-014-5883-4.
40. Lemire J, Alhasawi A, Appanna VP, Tharmalingam S, Appanna VD. 2017. Metabolic defence against oxidative stress: the road less travelled so far. J Appl Microbiol 123:798–809. https://doi.org/10.1111/jam.13509.
41. Singh R, Mailloux RJ, Puiseux-Dao S, Appanna VD. 2007. Oxidative stress evokes a metabolic adaptation that favors increased NADPH synthesis and decreased NADH production in Pseudomonas fluorescens. J Bacteriol 189:6665–6675. https://doi.org/10.1128/JB.00555-07.
42. Comini MA. 2016. Measurement and meaning of cellular thiol:disulfide redox status. Free Radic Res 50:246–271. https://doi.org/10.3109/1071 5762.2015.1110241.
43. Tamburro A, Robuffo I, Heipieper HJ, Allocati N, Rotilio D, Di Ilio C, Favaloro B. 2004. Expression of glutathione S-transferase and peptide methionine sulphoxide reductase in Ochrobactrum anthropi is correlated to the production of reactive oxygen species caused by aromatic substrates. FEMS Microbiol Lett 241:151–156. https://doi.org/10.1016/j.femsle.2004.10.013.
44. Nikel PI, Chavarría M, Danchin A, de Lorenzo V. 2016. From dirt to industrial applications: Pseudomonas putida as a synthetic biology chassis for hosting harsh biochemical reactions. Curr Opin Chem Biol 34:20–29. https://doi.org/10.1016/j.cbpa.2016.05.011.
45. Calero P, Nikel PI. 21 June 2018. Chasing bacterial chassis for metabolic engineering: a perspective review from classical to non-traditional microorganisms. Microb Biotechnol https://doi.org/10.1111/1751-7915.13292.
46. Gomez JGC, Méndez BS, Nikel PI, Pettinari MJ, Prieto MA, Silva LF. 2012. Making green polymers even greener: towards sustainable production of polyhydroxyalkanoates from agroindustrial by-products, p 41–62. In Petre M (ed), Advances in applied biotechnology. InTech, Rijeka, Croatia.
47. Nikel PI, Chavarría M, Fuhrer T, Sauer U, de Lorenzo V. 2015. Pseudomonas putida KT2440 strain metabolizes glucose through a cycle formed by enzymes of the Entner-Doudoroff, Embden-Meyerhof-Parnas, and pentose phosphate pathways. J Biol Chem 290:25920–25932. https://doi.org/10.1074/jbc.M115.687749.
48. Nikel PI, Chavarría M. 2016. Quantitative physiology approaches to understand and optimize reducing power availability in environmental bacteria, p 39–70. In McGenity TJ, Timmis KN, Nogales-Fernández B (ed), Hydrocarbon and lipid microbiology protocols–synthetic and systems biology–tools. Humana Press, Heidelberg, Germany. https://doi.org/10.1007/8623_2015_84.
49. Nikel PI, Pérez-Pantoja D, de Lorenzo V. 2016. Pyridine nucleotide transhydrogenases enable redox balance of Pseudomonas putida during biodegradation of aromatic compounds. Environ Microbiol 18: 3565–3582. https://doi.org/10.1111/1462-2920.13434.
50. de las Heras A, Chavarría M, 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. https://doi.org/10.1111/j.1365-2958.2011.07825.x.
51. Martínez-García E, Jatsenko T, Kivisaar M, de Lorenzo V. 2015. Freeing Pseudomonas putida KT2440 of its proviral load strengthens endurance to environmental stresses. Environ Microbiol 17:76–90. https://doi.org/10.1111/1462-2920.12492.
52. Lieder S, Nikel PI, de Lorenzo V, Takors R. 2015. Genome reduction boosts heterologous gene expression in Pseudomonas putida. Microb Cell Fact 14:23. https://doi.org/10.1186/s12934-015-0207-7.
53. Haigler BE, Nishino SF, Spain JC. 1994. Biodegradation of 4-methyl-5-nitrocatechol by Pseudomonas sp. strain DNT. J Bacteriol 176: 3433–3437. https://doi.org/10.1128/jb.176.11.3433-3437.1994.
54. Haigler BE, Suen WC, Spain JC. 1996. Purification and sequence analysis of 4-methyl-5-nitrocatechol oxygenase from Burkholderia sp. strain DNT. J Bacteriol 178:6019–6024. https://doi.org/10.1128/jb.178.20.6019-6024.1996.
55. Bolton JL, Trush MA, Penning TM, Dryhurst G, Monks TJ. 2000. Role of quinones in toxicology. Chem Res Toxicol 13:135–160. https://doi.org/10.1021/tx9902082.
56. Silva-Rocha R, Martínez-García E, Calles B, Chavarría M, Arce-Rodríguez A, de las Heras A, Páez-Espino AD, Durante-Rodríguez G, Kim J, Nikel PI, Platero R, de Lorenzo V. 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. https://doi.org/10.1093/nar/gks1119.
57. Galvão TC, de Lorenzo V. 2005. Adaptation of the yeast URA3 selection system to Gram-negative bacteria and generation of a ΔbetCDE Pseudomonas putida strain. Appl Environ Microbiol 71:883–892. https://doi.org/10.1128/AEM.71.2.883-892.2005.
58. Martínez-García E, Nikel PI, Aparicio T, de Lorenzo V. 2014. Pseudomonas 2.0: genetic upgrading of P. putida KT2440 as an enhanced host for heterologous gene expression. Microb Cell Fact 13:159. https://doi.org/10.1186/s12934-014-0159-3.
59. Drlica K, Zhao X. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61:377–392.
60. Harms A, Maisonneuve E, Gerdes K. 2016. Mechanisms of bacterial persistence during stress and antibiotic exposure. Science 354:aaf4268. https://doi.org/10.1126/science.aaf4268.
61. Baharoglu Z, Mazel D. 2014. SOS, the formidable strategy of bacteria against aggressions. FEMS Microbiol Rev 38:1126–1145. https://doi.org/10.1111/1574-6976.12077.
62. Abella M, Campoy S, Erill I, Rojo F, Barbé J. 2007. Cohabitation of two different lexA regulons in Pseudomonas putida. J Bacteriol 189: 8855–8862. https://doi.org/10.1128/JB.01213-07.
63. Benedetti IM, de Lorenzo V, 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. https://doi.org/10.1371/journal.pone.0052000.
64. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S, Goldfarb A, Darst SA. 2001. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104:901–912. https://doi.org/10.1016/S0092-8674(01)00286-0.
65. R mutations in Pseudomonas aeruginosa and Pseudomonas putida. Mutat Res 683:106–114. https://doi.org/10.1016/j.mrfmmm.2009.10.015.
66. Artsimovitch I, Vassylyeva MN, Svetlov D, Svetlov V, Perederina A, Igarashi N, Matsugaki N, Wakatsuki S, Tahirov TH, Vassylyev DG. 2005. Allosteric modulation of the RNA polymerase catalytic reaction is an essential component of transcription control by rifamycins. Cell 122: 351–363. https://doi.org/10.1016/j.cell.2005.07.014.
67. Nikel PI, Chavarría M, Martínez-García E, Taylor AC, de Lorenzo V. 2013. Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440. Microb Cell Fact 12:50. https://doi.org/10.1186/1475-2859-12-50.
68. Nikel PI, Romero-Campero FJ, Zeidman JA, Goñi-Moreno Á, de Lorenzo V. 2015. The glycerol-dependent metabolic persistence of Pseudomonas putida KT2440 reflects the regulatory logic of the GlpR repressor. mBio 6:e00340-15. https://doi.org/10.1128/mBio.00340-15.
69. Nikel PI, de Lorenzo V. 2014. Robustness of Pseudomonas putida KT2440 as a host for ethanol biosynthesis. New Biotechnol 31:562–571. https://doi.org/10.1016/j.nbt.2014.02.006.
70. Mishra S, Imlay J. 2012. Why do bacteria use so many enzymes to scavenge hydrogen peroxide? Arch Biochem Biophys 525:145–160. https://doi.org/10.1016/j.abb.2012.04.014.
71. + levels. J Bacteriol 196:2166–2177. https://doi.org/10.1128/JB.01542-14.
72. Tachon S, Chambellon E, Yvon M. 2011. Identification of a conserved sequence in flavoproteins essential for the correct conformation and activity of the NADH oxidase NoxE of Lactococcus lactis. J Bacteriol 193:3000–3008. https://doi.org/10.1128/JB.01466-10.
73. Ebert BE, Kurth F, Grund M, Blank LM, Schmid A. 2011. Response of Pseudomonas putida KT2440 to increased NADH and ATP demand. Appl Environ Microbiol 77:6597–6605. https://doi.org/10.1128/AEM.05588-11.
74. Benedetti I, de Lorenzo V, Nikel PI. 2016. Genetic programming of catalytic Pseudomonas putida biofilms for boosting biodegradation of haloalkanes. Metab Eng 33:109–118. https://doi.org/10.1016/j.ymben.2015.11.004.
75. Benedetti I, Nikel PI, de Lorenzo V. 2016. Data on the standardization of a cyclohexanone-responsive expression system for Gram-negative bacteria. Data Brief 6:738–744. https://doi.org/10.1016/j.dib.2016.01.022.
76. Moriya M, Grollman AP. 1993. Mutations in the mutY gene of Escherichia coli enhance the frequency of targeted G:C¡T:A transversions induced by a single 8-oxoguanine residue in single-stranded DNA. Mol Gen Genet 239:72–76. https://doi.org/10.1007/bf00281603.
77. Ohmori H, Friedberg EC, Fuchs RPP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, Prakash L, Prakash S, Todo T, Walker GC, Wang Z, Woodgate R. 2001. The Y-family of DNA polymerases. Mol Cell 8:7–8. https://doi.org/10.1016/S1097-2765(01)00278-7.
78. Jatsenko T, Sidorenko J, Saumaa S, Kivisaar M. 2017. DNA polymerases ImuC and DinB are involved in DNA alkylation damage tolerance in Pseudomonas aeruginosa and Pseudomonas putida. PLoS One 12: e0170719. https://doi.org/10.1371/journal.pone.0170719.
79. Thomas CM, Nielsen KM. 2005. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721. https://doi.org/10.1038/nrmicro1234.
80. Soucy SM, Huang J, Gogarten JP. 2015. Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482. https://doi.org/10.1038/nrg3962.
81. Koonin EV. 2016. Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res 5:1805. https://doi.org/10.12688/f1000research.8737.1.
82. Tarassova K, Tegova R, Tover A, Teras R, Tark M, Saumaa S, Kivisaar M. 2009. Elevated mutation frequency in surviving populations of carbon-starved rpoS-deficient Pseudomonas putida is caused by reduced expression of superoxide dismutase and catalase. J Bacteriol 191: 3604–3614. https://doi.org/10.1128/JB.01803-08.
83. Tavita K, Mikkel K, Tark-Dame M, Jerabek H, Teras R, Sidorenko J, Tegova R, Tover A, Dame RT, Kivisaar M. 2012. Homologous recombination is facilitated in starving populations of Pseudomonas putida by phenol stress and affected by chromosomal location of the recombination target. Mutat Res 737:12–24. https://doi.org/10.1016/j.mrfmmm.2012.07.004.
84. Bowman LAH, McLean S, Poole RK, Fukuto JM. 2011. The diversity of microbial responses to nitric oxide and agents of nitrosative stress: close cousins but not identical twins. Adv Microb Physiol 59:135–219. https://doi.org/10.1016/B978-0-12-387661-4.00006-9.
85. Cadet J, Douki T, Gasparutto D, Ravanat JL. 2003. Oxidative damage to DNA: formation, measurement and biochemical features. Mutat Res 531:5–23. https://doi.org/10.1016/j.mrfmmm.2003.09.001.
86. Ferraro DJ, Gakhar L, Ramaswamy S. 2005. Rieske business: structure-function of Rieske non-heme oxygenases. Biochem Biophys Res Commun 338:175–190. https://doi.org/10.1016/j.bbrc.2005.08.222.
87. Fuchs G, Boll M, Heider J. 2011. Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol 9:803–816. https://doi.org/10.1038/nrmicro2652.
88. Danchin A, Binder PM, Noria S. 2011. Antifragility and tinkering in biology (and in business) flexibility provides an efficient epigenetic way to manage risk. Genes 2:998–1016. https://doi.org/10.3390/genes 2040998.
89. Calabrese EJ, Baldwin LA. 2003. Hormesis: the dose-response revolution. Annu Rev Pharmacol Toxicol 43:175–197. https://doi.org/10.1146/annurev.pharmtox.43.100901.140223.
90. Calabrese EJ. 2005. Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 138:379–411. https://doi.org/10.1016/j.envpol.2004.10.001.
91. Gems D, Partridge L. 2008. Stress-response hormesis and aging: “that which does not kill us makes us stronger”. Cell Metab 7:200–203. https://doi.org/10.1016/j.cmet.2008.01.001.
92. Mattson MP. 2008. Hormesis defined. Ageing Res Rev 7:1–7. https://doi.org/10.1016/j.arr.2007.08.007.
93. Migliore L, Rotini A, Thaller MC. 2013. Low doses of tetracycline trigger the E. coli growth: A case of hormetic response. Dose-Response 11: 565–572. https://doi.org/10.2203/dose-response.13-002.Migliore.
94. Mathieu A, Fleurier S, Frénoy A, Dairou J, Bredeche MF, Sanchez-Vizuete P, Song X, Matic I. 2016. Discovery and function of a general core hormetic stress response in E. coli induced by sublethal concentrations of antibiotics. Cell Rep 17:46–57. https://doi.org/10.1016/j.celrep.2016.09.001.
95. Sun H, Calabrese EJ, Zheng M, Wang D, Pan Y, Lin Z, Liu Y. 2018. A swinging seesaw as a novel model mechanism for time-dependent hormesis under dose-dependent stimulatory and inhibitory effects: A case study on the toxicity of antibacterial chemicals to Aliivibrio fischeri. Chemosphere 205:15–23. https://doi.org/10.1016/j.chemosphere.2018.04.043.
96. Chávez FP, Lünsdorf H, Jérez CA. 2004. Growth of polychlorinated-biphenyl-degrading bacteria in the presence of biphenyl and chloro-biphenyls generates oxidative stress and massive accumulation of inorganic polyphosphate. Appl Environ Microbiol 70:3064–3072. https://doi.org/10.1128/AEM.70.5.3064-3072.2004.
97. Czechowska K, van der Meer JR. 2012. Reversible and irreversible pollutant-induced bacterial cellular stress effects measured by ethidium bromide uptake and efflux. Environ Sci Technol 46: 1201–1208. https://doi.org/10.1021/es203352y.
98. Kanaly RA, Harayama S. 2010. Advances in the field of high-molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microb Biotechnol 3:136–164. https://doi.org/10.1111/j.1751-7915.2009.00130.x.
99. Kang YS, Lee Y, Jung H, Jeon CO, Madsen EL, Park W. 2007. Overex-pressing antioxidant enzymes enhances naphthalene biodegradation in Pseudomonas sp. strain As1. Microbiology 153:3246–3254. https://doi.org/10.1099/mic.0.2007/008896-0.
100. Nikel PI, de Lorenzo V. 2018. Pseudomonas putida as a functional chassis for industrial biocatalysis: from native biochemistry to trans-metabolism. Metab Eng https://doi.org/10.1016/j.ymben.2018.05.005.
101. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor.
102. Martínez-García E, de Lorenzo V. 2012. Transposon-based and plasmid-based genetic tools for editing genomes of Gram-negative bacteria. Methods Mol Biol 813:267–283. https://doi.org/10.1007/978-1-61779-412-4_16.
103. Nikel PI, Kim J, de Lorenzo V. 2014. Metabolic and regulatory rearrangements underlying glycerol metabolism in Pseudomonas putida KT2440. Environ Microbiol 16:239–254. https://doi.org/10.1111/1462-2920.12224.
104. Foster PL. 2005. Stress responses and genetic variation in bacteria. Mutat Res 569:3–11. https://doi.org/10.1016/j.mrfmmm.2004.07.017.
105. Rosche WA, Foster PL. 2000. Determining mutation rates in bacterial populations. Methods 20:4–17. https://doi.org/10.1006/meth.1999.0901.
106. Martínez-García E, Aparicio T, de Lorenzo V, Nikel PI. 2014. New transposon tools tailored for metabolic engineering of Gram-negative microbial cell factories. Front Bioeng Biotechnol 2:46. https://doi.org/10.3389/fbioe.2014.00046.
107. Nikel PI, de Lorenzo V. 2013. Implantation of unmarked regulatory and metabolic modules in Gram-negative bacteria with specialised mini-transposon delivery vectors. J Biotechnol 163:143–154. https://doi.org/10.1016/j.jbiotec.2012.05.002.
108. Nikel PI, de Lorenzo V. 2013. Engineering an anaerobic metabolic regime in Pseudomonas putida KT2440 for the anoxic biodegradation of 1,3-dichloroprop-1-ene. Metab Eng 15:98–112. https://doi.org/10.1016/j.ymben.2012.09.006.
109. Dvořák P, Chrást L, Nikel PI, Fedr R, Soucek K, Sedlacková M, Chaloup-ková R, de Lorenzo V, Prokop Z, Damborský J. 2015. Exacerbation of substrate toxicity by IPTG in Escherichia coli BL21(DE3) carrying a synthetic metabolic pathway. Microb Cell Fact 14:201. https://doi.org/10.1186/s12934-015-0393-3.
110. Couce A, Blázquez J. 2009. Side effects of antibiotics on genetic variability. FEMS Microbiol Rev 33:531–538. https://doi.org/10.1111/j.1574-6976.2009.00165.x.