Genetics of Sensing, Accessing, and Exploiting Hydrocarbons

  1. Matilla, Miguel A. 2
  2. Daniels, Craig
  3. del Castillo, Teresa 3
  4. Busch, Andreas
  5. Lacal, Jesús 1
  6. Segura, Ana 2
  7. Ramos, Juan Luis 2
  8. Krell, Tino 2
  1. 1 Universidad de Salamanca
    info

    Universidad de Salamanca

    Salamanca, España

    ROR https://ror.org/02f40zc51

  2. 2 Estación Experimental del Zaidín
    info

    Estación Experimental del Zaidín

    Granada, España

    ROR https://ror.org/00drcz023

  3. 3 Universidad de Granada
    info

    Universidad de Granada

    Granada, España

    ROR https://ror.org/04njjy449

Mostrar afiliaciones +
Libro:
Cellular Ecophysiology of Microbe: Hydrocarbon and Lipid Interactions

Editorial: Cham : Springer International Publishing

ISBN: 978-3-319-50540-4

Año de publicación: 2018

Páginas: 345-359

Tipo: Capítulo de Libro

DOI: 10.1007/978-3-319-50542-8_46 GOOGLE SCHOLAR lock_openAcceso abierto editor

Objetivos de desarrollo sostenible

Resumen

Hydrocarbons abound in the environment and microorganisms are often capable of detecting, assimilating, and degrading these normally recalcitrant molecules. In order to achieve this, bacteria have developed specific sensor proteins and adaptive mechanisms. In the presence of hydrocarbons, the bacterial adaptive response is modulated at the transcriptional and post-transcriptional levels by one- and two-component regulatory systems, global regulators, and DNA-binding proteins. The expressed gene products are then able to degrade the molecules and often take advantage of the stored energy imparted by the physicochemical properties of the hydrocarbon structure. The response of regulators to the presence of hydrocarbons such as toluene in the environment allows initiation or inhibition of transcription, so that the rate of synthesis of metabolically important gene products is adaptively modulated. Microorganisms which mount the most appropriate physiological adaptation are then able to proliferate in the changing environment. Here, we give an overview of the bacterial chemotactic responses towards hydrocarbons and the adaptive regulation of catabolic pathways responsible for the degradation of aromatic hydrocarbons. The use of microorganisms with biodegradative capabilities offers an environmentally friendly alternative for the treatment of hydrocarbon-contaminated environments.

Referencias bibliográficas

  • Aranda-Olmedo I, Ramos JL, Marqués S (2005) Integration of signals through Crc and PtsN in catabolite repression of Pseudomonas putida TOL plasmid pWW0. Appl Environ Microbiol 71:4191–4198
  • Aranda-Olmedo I, Marín P, Ramos JL, Marqués S (2006) Role of the ptsN gene product in catabolite repression of the Pseudomonas putida TOL toluene degradation pathway in chemostat cultures. Appl Environ Microbiol 72:7418–7721
  • Baumgarten T, Vazquez J, Bastisch C, Veron W, Feuilloley MG, Nietzsche S, Wick LY, Heipieper HJ (2012) Alkanols and chlorophenols cause different physiological adaptive responses on the level of cell surface properties and membrane vesicle formation in Pseudomonas putida DOT-T1E. Appl Microbiol Biotechnol 93:837–845
  • Busch A, Lacal J, Marcos A, Ramos JL, Krell T (2007) Bacterial sensor kinase TodS interacts with agonistic and antagonistic signals. Proc Natl Acad Sci U S A 104:13774–13779
  • Busch A, Guazzaroni ME, Lacal J, Ramos JL, Krell T (2009) The sensor kinase TodS operates by a multiple step phosphorelay mechanism involving two autokinase domains. J Biol Chem 284:10353–10360
  • Busch A, Lacal J, Silva-Jímenez H, Krell T, Ramos JL (2010) Catabolite repression of the TodS/TodT two-component system and effector-dependent transphosphorylation of TodT as the basis for toluene dioxygenase catabolic pathway control. J Bacteriol 192:4246–4250
  • Bush M, Dixon R (2012) The role of bacterial enhancer binding proteins as specialized activators of σ54-dependent transcription. Microbiol Mol Biol Rev 76:497–529
  • Capra EJ, Laub MT (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66:325–347
  • Collins KD, Lacal J, Ottemann KM (2014) Internal sense of direction: sensing and signaling from cytoplasmic chemoreceptors. Microbiol Mol Biol Rev 78:672–684
  • Dagley S (1981) New perspectives in aromatic catabolism. In: Leisinger T, Cook AM, Hütter R, Nüesch J (eds) Degradation of xenobiotics and recalcitrant compounds. Academic Press, New York, pp 181–186
  • del Castillo T, Ramos JL (2007) Simultaneous catabolite repression between glucose and toluene metabolism in Pseudomonas putida is channelled through different signalling pathways. J Bacteriol 189:6602–6610
  • Domínguez-Cuevas P, Marqués S (2004) Compiling sigma-70 dependent promoters. In: Ramos JL (ed) Pseudomonas: virulence and gene regulation. Springer, New York, pp 319–345
  • Duetz WA, Marqués S, Wind B, Ramos JL, van Andel JG (1996) Catabolite repression of the toluene degradation pathway in Pseudomonas putida harboring pWW0 under various conditions of nutrient limitation in chemostat culture. Appl Environ Microbiol 62:601–606
  • Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds – from one strategy to four. Nat Rev Microbiol 9:803–816
  • Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98:4781–4794
  • Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL (1997) Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61:393–410
  • Galperin MY (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 5:35
  • Gibson DT, Subramanian V (1984) Microbial degradation of aromatic hydrocarbons. In: Gibson DT (ed) Microbial degradation of organic compounds. Marcel Dekker, New York, pp 361–369
  • Grimm AC, Harwood CS (1997) Chemotaxis of Pseudomonas spp. to the polyaromatic hydrocarbon naphthalene. Appl Environ Microbiol 63:4111–4115
  • Grimm AC, Harwood CS (1999) NahY, a catabolic plasmid-encoded receptor required for chemotaxis of Pseudomonas putida to the aromatic hydrocarbon naphthalene. J Bacteriol 181:3310–3316
  • Harwood CS, Rivelli M, Ornston LN (1984) Aromatic acids are chemoattractants for Pseudomonas putida. J Bacteriol 160:622–628
  • Harwood CS, Parales RE, Dispensa M (1990) Chemotaxis of Pseudomonas putida toward chlorinated benzoates. Appl Environ Microbiol 56:1501–1503
  • Hearn EM, Patel DR, van den Berg B (2008) Outer-membrane transport of aromatic hydrocarbons as a first step in biodegradation. Proc Natl Acad Sci U S A 105:8601–8606
  • Huang Z, Ni B, Jiang CY, Wu YF, He YZ, Parales RE, Liu SJ (2016) Direct sensing and signal transduction during bacterial chemotaxis towards aromatic compounds in Comamonas testosteroni. Molecular Microbiology 101(2):224–237. https://doi.org/10.1111/mmi.13385
  • Inoue A, Horikoshi K (1989) A Pseudomonas that thrives in high concentration of toluene. Nature 338:264–266
  • Kim J, Pérez-Pantoja D, Silva-Rocha R, Oliveros JC, de Lorenzo V (2016) High-resolution analysis of the m-xylene/toluene biodegradation subtranscriptome of Pseudomonas putida mt-2. Environ Microbiol. Environ Microbiol 18(10):3327–3341. https://doi.org/10.1111/1462-2920.13054
  • Koh S, Hwang J, Guchhait K, Lee EG, Kim SY, Kim S, Lee S, Chung JM, Jung HS, Lee SJ, Ryu CM, Lee SG, TK O, Kwon O, Kim MH (2016) Molecular insights into toluene sensing in the TodS/TodT signal transduction system. J Biol Chem 291:8575–8590
  • Krell T, Lacal J, Busch A, Silva-Jiménez H, Guazzaroni ME, Ramos JL (2010) Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64:539–559
  • Krell T, Lacal J, Guazzaroni ME, Busch A, Silva-Jiménez H, Fillet S, Reyes-Darías JA, Muñoz-Martínez F, Rico-Jiménez M, García-Fontana C, Duque E, Segura A, Ramos JL (2012) Responses of Pseudomonas putida to toxic aromatic carbón sources. J Biotechnol 160:25–32
  • Kremling A, Geiselmann J, Ropers D, de Jong H (2015) Understanding carbon catabolite repression in Escherichia coli using quantitative models. Trends Microbiol 23:99–109
  • Lacal J, Busch A, Guazzaroni ME, Krell T, Ramos JL (2006) The TodS–TodT two-component regulatory system recognizes a wide range of effectors and works with DNA-bending proteins. Proc Natl Acad Sci U S A 103:8191–8196
  • Lacal J, Guazzaroni ME, Busch A, Krell T, Ramos JL (2008a) Hierarchical binding of the TodT response regulator to its multiple recognition sites at the tod pathway operon promoter. J Mol Biol 376:325–337
  • Lacal J, Guazzaroni ME, Gutiérrez-del-Arroyo P, Busch A, Vélez M, Krell T, Ramos JL (2008b) Two levels of cooperativeness in the binding of TodT to the tod operon promoter. J Mol Biol 384:1037–1047
  • Lacal J, Muñoz-Martínez F, Reyes-Darías JA, Duque E, Matilla M, Segura A, Calvo JJ, Jímenez-Sánchez C, Krell T, Ramos JL (2011) Bacterial chemotaxis towards aromatic hydrocarbons in Pseudomonas. Environ Microbiol 13:1733–1744
  • Lacal J, Reyes-Darias JA, García-Fontana C, Ramos JL, Krell T (2013) Tactic responses to pollutants and their potential to increase biodegradation efficiency. J Appl Microbiol 114:923–933
  • Lau PC, Wang Y, Patel A, Labbé D, Bergeron H, Brousseau R, Konishi Y, Rawlings M (1997) A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc Natl Acad Sci U S A 94:1453–1458
  • Law AM, Aitken MD (2003) Bacterial chemotaxis to naphthalene desorbing from a nonaqueous liquid. Appl Environ Microbiol 69:5968–5973
  • Leoni L, Rampioni G, Zennaro E (2007) Styrene, an unpalatable substrate with complex regulatory networks. In: Ramos JL, Filloux A (eds) Pseudomonas: a model system in biology. Springer, Dorchester, pp 59–88
  • Maddocks SE, Oyston PC (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154:3609–3623
  • Marqués S, Gallegos MT, Manzanera M, Holtel A, Timmis KN, Ramos JL (1998) Activation and repression of transcription at the double tandem divergent promoters for the xylR and xylS genes of the TOL plasmid of Pseudomonas putida. J Bacteriol 180:2889–2894
  • Marx RB, Aitken MD (2000a) Bacterial chemotaxis enhances naphthalene degradation in a heterogeneous system. Environ Sci Technol 34:3379–3383
  • Marx RB, Aitken MD (2000b) A material-balance approach for modeling bacterial chemotaxis to a consumable substrate in the capillary assay. Biotechnol Bioeng 68:308–315
  • Molina L, Duque E, Gómez MJ, Krell T, Lacal J, García-Puente A, García V, Matilla MA, Ramos JL, Segura A (2011) The pGRT1 plasmid of Pseudomonas putida DOT-T1E encodes functions relevant for survival under harsh conditions in the environment. Environ Microbiol 13:2315–2327
  • Moreno R, Fonseca P, Rojo F (2010) The Crc global regulator inhibits the Pseudomonas putida pWW0 toluene/xylene assimilation pathway by repressing the translation of regulatory and structural genes. J Biol Chem 285:24412–24419
  • Mosqueda G, Ramos-González MI, Ramos JL (1999) Toluene metabolism by the solvent-tolerant Pseudomonas putida DOT-T1 strain, and its role in solvent impermeabilization. Gene 232:69–76
  • Parales RE, Ditty JL, Harwood CS (2000) Toluene-degrading bacteria are chemotactic towards the environmental pollutants benzene, toluene, and trichloroethylene. Appl Environ Microbiol 66:4098–4104
  • Parales RE, Parales JV, Pelletier DA, Ditty JL (2008) Diversity of microbial toluene degradation pathways. Adv Appl Microbiol 64:1–73
  • Parales RE, Luu RA, Hughes JG, Ditty JL (2015) Bacterial chemotaxis to xenobiotic chemicals and naturally-occurring analogs. Curr Opin Biotechnol 33:318–326
  • Parkinson JS, Hazelbauer GL, Falke JJ (2015) Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. Trends Microbiol 23:257–266
  • Phillips AT, Mulfinger LM (1981) Cyclic adenosine 3′,5′-monophosphate levels in Pseudomonas putida and Pseudomonas aeruginosa during induction and carbon catabolite repression of histidase synthesis. J Bacteriol 145:1286–1292
  • Piñar G, Kovárová K, Egli T, Ramos JL (1998) Influence of carbon source of nitrate removal by nitratetolerant Klebsiella oxytoca CECT 4460 in batch and chemostat cultures. Appl Environ Microbiol 64:2970–2976
  • Pohanish RP (2011) Sittig’s handbook of toxic and hazardous chemicals and carcinogens, 6th edn. William Andrew-Elsevier, Norwich
  • Ramos JL, Duque E, Huertas MJ, Haïdour A (1995) Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high concentrations of aromatic hydrocarbons. J Bacteriol 177:3911–3916
  • Ramos JL, Marqués S, Timmis KN (1997) Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators. Annu Rev Microbiol 51:341–373
  • Ramos JL, Duque E, van Dillewjin P, Daniels C, Krell T, Espinosa-Urgel M, Ramos-González MI, Rodríguez S, Matilla MA, Wittich R, Segura A (2010) Removal of hydrocarbons and other related chemicals via the rhizosphere of plants. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2575–2581
  • Ramos JL, Sol Cuenca M, Molina-Santiago C, Segura A, Duque E, Gómez-García MR, Udaondo Z, Roca A (2015) Mechanisms of solvent resistance mediated by interplay of cellular factors in Pseudomonas putida. FEMS Microbiol Rev 39:555–566
  • Rojo F, Dinamarca A (2004) Catabolite repression and physiological control. In: Ramos JL (ed) Pseudomonas: virulence and gene regulation. Springer, New York, pp 365–387
  • Sampedro I, Parales RE, Krell T, Hill JE (2015) Pseudomonas chemotaxis. FEMS Microbiol Rev 39:17–46
  • Segura A, Ramos JL (2014) Toluene tolerance systems in Pseudomonas. In: Nojiri H, Tsuda M, Fukuda M, Kamagata Y (eds) Biodegradative bacteria: how bacteria degrade, survive, adapt, and evolve. Springer, Tokyo, pp 227–248
  • Segura A, Molina L, Fillet S, Krell T, Bernal P, Muñoz-Rojas J, Ramos JL (2012) Solvent tolerance in Gram-negative bacteria. Curr Opin Biotechnol 23:415–421
  • Silva-Jiménez H, García-Fontana C, Cadirci BH, Ramos-González MI, Ramos JL, Krell T (2012) Study of the TmoS/TmoT two-component system: towards the functional characterization of the family of TodS/TodT like systems. Microb Biotechnol 5:489–500
  • Silva-Rocha R, Tamames J, dos Santos VM, de Lorenzo V (2011) The logicome of environmental bacteria: merging catabolic and regulatory events with Boolean formalisms. Environ Microbiol 13:2389–2402
  • Udaondo Z, Duque E, Fernández M, Molina L, de la Torre J, Bernal P, Niqui JL, Pini C, Roca A, Matilla MA, Molina-Henares MA, Silva-Jiménez H, Navarro-Avilés G, Busch A, Lacal J, Krell T, Segura A, Ramos JL (2012) Analysis of solvent tolerance in Pseudomonas putida DOT-T1E based on its genome sequence and a collection of mutants. FEBS Lett 586:2932–2938
  • Udaondo Z, Molina L, Daniels C, Gómez MJ, Molina-Henares MA, Matilla MA, Roca A, Fernández M, Duque E, Segura A, Ramos JL (2013) Metabolic potential of the organic-solvent tolerant Pseudomonas putida DOT-T1E deduced from its annotated genome. Microb Biotechnol 6:598–611
  • Worsey MJ, Williams PA (1975) Metabolism of toluene and xylenes by Pseudomonas (putida (arvilla) mt-2: evidence for a new function of the TOL plasmid. J Bacteriol 124:7–13
  • Wuichet K, Cantwell BJ, Zhulin IB (2010) Evolution and phyletic distribution of two-component signal transduction systems. Curr Opin Microbiol 13:219–225
  • Zylstra GJ, McCombie WR, Gibson DT, Finette BA (1988) Toluene degradation by Pseudomonas putida F1: genetic organization of the tod operon. Appl Environ Microbiol 54:1498–1503