Transcriptional control of 2,4-dinitrotoluene degradation in Burkholderia sp. R34 bears a regulatory patch that eases pathway evolution.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
revised:
27
02
2021
received:
07
12
2020
accepted:
16
03
2021
pubmed:
19
3
2021
medline:
16
10
2021
entrez:
18
3
2021
Statut:
ppublish
Résumé
The dnt pathway of Burkholderia sp. R34 is in the midst of an evolutionary journey from its ancestral, natural substrate (naphthalene) towards a new xenobiotic one [2,4-dinitrotoluene (DNT)]. The gene cluster encoding the leading multicomponent ring dioxygenase (DntA) has activity on the old and the new substrate, but it is induced by neither. Instead, the transcriptional factor encoded by the adjacent gene (dntR) activates expression of the dnt cluster upon addition of salicylate, one degradation intermediate of the ancestral naphthalene route but not any longer a substrate/product of the evolved DntA enzyme. Fluorescence of cells bearing dntA-gfp fusions revealed that induction of the dnt genes by salicylate was enhanced upon exposure to bona fide DntA substrates, i.e., naphthalene or DNT. Such amplification was dependent on effective dioxygenation of these pathway-specific head compounds, which thereby fostered expression of the cognate catabolic operon. The phenomenon seems to happen not through direct binding to a cognate transcriptional factor but through the interplay of a non-specific regulator with a substrate-specific enzyme. This regulatory scenario may ease transition of complete catabolic operons (i.e. enzymes plus regulatory devices) from one substrate to another without loss of fitness during the evolutionary roadmap between two optimal specificities.
Identifiants
pubmed: 33734558
doi: 10.1111/1462-2920.15472
doi:
Substances chimiques
Dinitrobenzenes
0
2,4-dinitrotoluene
6741D310ED
Dioxygenases
EC 1.13.11.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2522-2531Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Abril, M.A., Michan, C., Timmis, K.N., and Ramos, J.L. (1989) Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway. J Bacteriol 171: 6782-6790.
Akkaya, Ö., Perez-Pantoja, D., Calles, B., Nikel, P.I., and de Lorenzo, V. (2018) The metabolic redox regime of Pseudomonas putida tunes its evolvability toward novel xenobiotic substrates. mBio 9: e01512-18.
Akkaya, Ö., Nikel, P.I., Perez-Pantoja, D., and de Lorenzo, V. (2019) Evolving metabolism of 2,4-dinitrotoluene triggers SOS-independent diversification of host cells. Environ Microbiol 21: 314-326.
Axler-Diperte, G.L., Miller, V.L., and Darwin, A.J. (2006) YtxR, a conserved LysR-like regulator that induces expression of genes encoding a putative ADP-ribosyltransferase toxin homologue in Yersinia enterocolitica. J Bacteriol 188: 8033-8043.
Cases, I., and de Lorenzo, V. (2001) The black cat/white cat principle of signal integration in bacterial promoters. EMBO J 20: 1-11.
de Las Heras, A., Chavarría, 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.
Devesse, L., Smirnova, I., Lonneborg, R., Kapp, U., Brzezinski, P., Leonard, G.A., and Dian, C. (2011) Crystal structures of DntR inducer binding domains in complex with salicylate offer insights into the activation of LysR-type transcriptional regulators. Mol Microbiol 81: 354-367.
Fuenmayor, S.L., Wild, M., Boyes, A.L., and Williams, P.A. (1998) A gene cluster encoding steps in conversion of naphthalene to gentisate in Pseudomonas sp. strain U2. J Bacteriol 180: 2522-2530.
Gibson, D.T., and Parales, R.E. (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11: 236-243.
Grob, P., and Guiney, D.G. (1996) In vitro binding of the Salmonella dublin virulence plasmid regulatory protein SpvR to the promoter regions of spvA and spvR. J Bacteriol 178: 1813-1820.
Floriano, B., Santero, E., and Reyes-Ramírez, F. (2019) Biodegradation of Tetralin: genomics, gene function and regulation. Genes (Basel) 10: 339.
Habe, H., and Omori, T. (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67: 225-243.
Harris, S.J., Shih, Y.L., Bentley, S.D., and Salmond, G.P. (1998) The hexA gene of Erwinia carotovora encodes a LysR homologue and regulates motility and the expression of multiple virulence determinants. Mol Microbiol 28: 705-717.
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.
Johnson, G.R., Jain, R.K., and Spain, J.C. (2000) Properties of the trihydroxytoluene oxygenase from Burkholderia cepacia R34: an extradiol dioxygenase from the 2,4-dinitrotoluene pathway. Arch Microbiol 173: 86-90.
Johnson, G.R., Jain, R.K., and Spain, J.C. (2002) Origins of the 2,4-dinitrotoluene pathway. J Bacteriol 184: 4219-4232.
Jones, R.M., Britt-Compton, B., and Williams, P.A. (2003) The naphthalene catabolic (nag) genes of Ralstonia sp. strain U2 are an operon that is regulated by NagR, a LysR-type transcriptional regulator. J Bacteriol 185: 5847-5853.
Ju, K.S., and Parales, R.E. (2010) Nitroaromatic compounds, from synthesis to biodegradation. Microbiol Mol Biol Rev 74: 250-272.
Kovacic, P., and Somanathan, R. (2014) Nitroaromatic compounds: environmental toxicity, carcinogenicity, mutagenicity, therapy and mechanism. J Appl Toxicol 34: 810-824.
Lehnen, D., Blumer, C., Polen, T., Wackwitz, B., Wendisch, V.F., and Unden, G. (2002) LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol Microbiol 45: 521-532.
Lessner, D.J., Johnson, G.R., Parales, R.E., Spain, J.C., and Gibson, D.T. (2002) Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765. Appl Environ Microbiol 68: 634-641.
Lonneborg, R., and Brzezinski, P. (2011) Factors that influence the response of the LysR type transcriptional regulators to aromatic compounds. BMC Biochem 12: 49.
Lonneborg, R., Varga, E., and Brzezinski, P. (2012) Directed evolution of the transcriptional regulator DntR: isolation of mutants with improved DNT-response. PLoS One 7: e29994.
Lonneborg, R., Smirnova, I., Dian, C., Leonard, G.A., and Brzezinski, P. (2007) In vivo and in vitro investigation of transcriptional regulation by DntR. J Mol Biol 372: 571-582.
Lopez-Sanchez, A., Rivas-Marin, E., Martinez-Perez, O., Floriano, B., and Santero, E. (2009) Co-ordinated regulation of two divergent promoters through higher-order complex formation by the LysR-type regulator ThnR. Mol Microbiol 73: 1086-1100.
Maddocks, S.E., and Oyston, P.C. (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154: 3609-3623.
Martinez-Perez, O., Lopez-Sanchez, A., Reyes-Ramirez, F., Floriano, B., and Santero, E. (2007) Integrated response to inducers by communication between a catabolic pathway and its regulatory system. J Bacteriol 189: 3768-3775.
Mason, J.R., and Cammack, R. (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 46: 277-305.
Mitchell, R.J., and Gu, M.B. (2005) Construction and evaluation of nagR-nagAa::lux fusion strains in biosensing for salicylic acid derivatives. Appl Biochem Biotechnol 120: 183-198.
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.
Parales, J.V., Kumar, A., Parales, R.E., and Gibson, D.T. (1996) Cloning and sequencing of the genes encoding 2-nitrotoluene dioxygenase from Pseudomonas sp. JS42. Gene 181: 57-61.
Parales, R.E., Huang, R., Yu, C.L., Parales, J.V., Lee, F.K.N., Lessner, D.J., et al. (2005) Purification, characterization, and crystallization of the components of the nitrobenzene and 2-nitrotoluene dioxygenase enzyme systems. Appl Environ Microbiol 71: 3806-3814.
Parry, R., Nishino, S., and Spain, J. (2011) Naturally-occurring nitro compounds. Nat Prod Rep 28: 152-167.
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.
Singh, D., Kumari, A., and Ramanathan, G. (2014) 3-Nitrotoluene dioxygenase from Diaphorobacter sp. strains: cloning, sequencing and evolutionary studies. Biodegradation 25: 479-492.
Smirnova, I.A., Dian, C., Leonard, G.A., McSweeney, S., Birse, D., and Brzezinski, P. (2004) Development of a bacterial biosensor for nitrotoluenes: the crystal structure of the transcriptional regulator DntR. J Mol Biol 340: 405-418.
Suen, W.C., and Spain, J.C. (1993) Cloning and characterization of Pseudomonas sp. strain DNT genes for 2,4-dinitrotoluene degradation. J Bacteriol 175: 1831-1837.
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.
Taghavi, S., van der Lelie, D., and Mergeay, M. (1994) Electroporation of Alcaligenes eutrophus with (mega) plasmids and genomic DNA fragments. Appl Environ Microbiol 60: 3585-3591.
Turner, K.H., Vallet-Gely, I., and Dove, S.L. (2009) Epigenetic control of virulence gene expression in Pseudomonas aeruginosa by a LysR-type transcription regulator. PLoS Genet 5: e1000779.
Wall, M.E., Hlavacek, W.S., and Savageau, M.A. (2004) Design of gene circuits: lessons from bacteria. Nat Rev Genet 5: 34-42.
Yin, S., Fuangthong, M., Laratta, W.P., and Shapleigh, J.P. (2003) Use of a green fluorescent protein-based reporter fusion for detection of nitric oxide produced by denitrifiers. Appl Environ Microbiol 69: 3938-3944.
Young, R.A. (2014) Dinitrotoluene. In Encyclopedia of Toxicology, 3rd ed, Wexler, P. (ed): Amsterdam: Academic Press, pp. 179-182.
Zhou, N.Y., Al-Dulayymi, J., Baird, M.S., and Williams, P.A. (2002) Salicylate 5-hydroxylase from Ralstonia sp. strain U2: a monooxygenase with close relationships to and shared electron transport proteins with naphthalene dioxygenase. J Bacteriol 184: 1547-1555.