1887

Abstract

Soil bacteria such as pseudomonads are widely studied due to their diverse metabolic capabilities, particularly the ability to degrade both naturally occurring and xenobiotic aromatic compounds. Chemotaxis, the directed movement of cells in response to chemical gradients, is common in motile soil bacteria and the wide range of chemicals detected often mirrors the metabolic diversity observed. Pseudomonas putida F1 is a soil isolate capable of chemotaxis toward, and degradation of, numerous aromatic compounds. We showed that P. putida F1 is capable of degrading members of a class of naturally occurring aromatic compounds known as hydroxycinnamic acids, which are components of lignin and are ubiquitous in the soil environment. We also demonstrated the ability of P. putida F1 to sense three hydroxycinnamic acids: p-coumaric, caffeic and ferulic acids. The chemotaxis response to hydroxycinnamic acids was induced during growth in the presence of hydroxycinnamic acids and was negatively regulated by HcaR, the repressor of the hydroxycinnamic acid catabolic genes. Chemotaxis to the three hydroxycinnamic acids was dependent on catabolism, as a mutant lacking the gene encoding feruloyl-CoA synthetase (Fcs), which catalyzes the first step in hydroxycinnamic acid degradation, was unable to respond chemotactically toward p-coumaric, caffeic, or ferulic acids. We tested whether an energy taxis mutant could detect hydroxycinnamic acids and determined that hydroxycinnamic acid sensing is mediated by the energy taxis receptor Aer2.

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2017-09-28
2019-10-15
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References

  1. Parales RE, Luu RA, Hughes JG, Ditty JL. Bacterial chemotaxis to xenobiotic chemicals and naturally-occurring analogs. Curr Opin Biotechnol 2015; 33: 318– 326 [CrossRef] [PubMed]
    [Google Scholar]
  2. Sampedro I, Parales RE, Krell T, Hill JE. Pseudomonas chemotaxis. FEMS Microbiol Rev 2015; 39: 17– 46
    [Google Scholar]
  3. Parales RE, Ferrandez A, Harwood CS. Chemotaxis in Pseudomonads. In Ramos J-L. (editor) Pseudomonas Volume I: Genomics, Life Style and Molecular Architechture New York: Kluwer Academic/Plenum Publishers; 2004; pp. 793– 815
    [Google Scholar]
  4. Lacal J, García-Fontana C, Muñoz-Martínez F, Ramos JL, Krell T. Sensing of environmental signals: classification of chemoreceptors according to the size of their ligand binding regions. Environ Microbiol 2010; 12: 2873– 2884 [CrossRef] [PubMed]
    [Google Scholar]
  5. Parkinson JS, Ames P, Studdert CA. Collaborative signaling by bacterial chemoreceptors. Curr Opin Microbiol 2005; 8: 116– 121 [CrossRef] [PubMed]
    [Google Scholar]
  6. Parales RE, Ditty JL, Harwood CS. Toluene-degrading bacteria are chemotactic towards the environmental pollutants benzene, toluene, and trichloroethylene. Appl Environ Microbiol 2000; 66: 4098– 4104 [CrossRef] [PubMed]
    [Google Scholar]
  7. Luu RA, Schneider BJ, Ho CC, Nesteryuk V, Ngwesse SE et al. Taxis of Pseudomonas putida F1 toward phenylacetic acid is mediated by the energy taxis receptor Aer2. Appl Environ Microbiol 2013; 79: 2416– 2423 [CrossRef] [PubMed]
    [Google Scholar]
  8. Luu RA, Kootstra JD, Nesteryuk V, Brunton CN, Parales JV et al. Integration of chemotaxis, transport and catabolism in Pseudomonas putida and identification of the aromatic acid chemoreceptor PcaY. Mol Microbiol 2015; 96: 134– 147 [CrossRef] [PubMed]
    [Google Scholar]
  9. Taofiq O, González-Paramás AM, Barreiro MF, Ferreira IC. Hydroxycinnamic acids and their derivatives: cosmeceutical significance, challenges and future perspectives, a review. Molecules 2017; 22: 281 [CrossRef]
    [Google Scholar]
  10. Douglas CJ. Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees. Trends Plant Sci 1996; 1: 171– 178 [CrossRef]
    [Google Scholar]
  11. Lewis NG, Yamamoto E. Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 1990; 41: 455– 496 [CrossRef] [PubMed]
    [Google Scholar]
  12. Campillo T, Renoud S, Kerzaon I, Vial L, Baude J et al. Analysis of hydroxycinnamic acid degradation in Agrobacterium fabrum reveals a coenzyme A-dependent, beta-oxidative deacetylation pathway. Appl Environ Microbiol 2014; 80: 3341– 3349 [CrossRef] [PubMed]
    [Google Scholar]
  13. Narbad A, Gasson MJ. Metabolism of ferulic acid via vanillin using a novel CoA-dependent pathway in a newly-isolated strain of Pseudomonas fluorescens. Microbiology 1998; 144: 1397– 1405 [CrossRef] [PubMed]
    [Google Scholar]
  14. Otani H, Lee YE, Casabon I, Eltis LD. Characterization of p-hydroxycinnamate catabolism in a soil Actinobacterium. J Bacteriol 2014; 196: 4293– 4303 [CrossRef] [PubMed]
    [Google Scholar]
  15. Overhage J, Priefert H, Steinbüchel A. Biochemical and genetic analyses of ferulic acid catabolism in Pseudomonas sp. strain HR199. Appl Environ Microbiol 1999; 65: 4837– 4847 [PubMed]
    [Google Scholar]
  16. Plaggenborg R, Steinbüchel A, Priefert H. The coenzyme A-dependent, non-β-oxidation pathway and not direct deacetylation is the major route for ferulic acid degradation in Delftia acidovorans. FEMS Microbiol Lett 2001; 205: 9– 16 [PubMed]
    [Google Scholar]
  17. Lowe TM, Ailloud F, Allen C. Hydroxycinnamic acid degradation, a broadly conserved trait, protects Ralstonia solanacearum from chemical plant defenses and contributes to root colonization and virulence. Mol Plant Microbe Interact 2015; 28: 286– 297 [CrossRef] [PubMed]
    [Google Scholar]
  18. Venturi V, Zennaro F, Degrassi G, Okeke BC, Bruschi CV. Genetics of ferulic acid bioconversion to protocatechuic acid in plant-growth-promoting Pseudomonas putida WCS358. Microbiology 1998; 144: 965– 973 [CrossRef] [PubMed]
    [Google Scholar]
  19. Kallscheuer N, Vogt M, Kappelmann J, Krumbach K, Noack S et al. Identification of the phd gene cluster responsible for phenylpropanoid utilization in Corynebacterium glutamicum. Appl Microbiol Biotechnol 2016; 100: 1871– 1881 [CrossRef] [PubMed]
    [Google Scholar]
  20. Kape R, Parniske M, Werner D. Chemotaxis and nod gene activity of Bradyrhizobium japonicum in response to hydroxycinnamic acids and isoflavonoids. Appl Environ Microbiol 1991; 57: 316– 319 [PubMed]
    [Google Scholar]
  21. Sambrook J, Fritch EF, Maniatis T. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory; 1989
    [Google Scholar]
  22. Stanier RY, Palleroni NJ, Doudoroff M. The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 1966; 43: 159– 271 [CrossRef] [PubMed]
    [Google Scholar]
  23. Simon R, Priefer U, Pühler A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Biotechnology 1983; 1: 784– 791 [CrossRef]
    [Google Scholar]
  24. Parkinson JS. A "bucket of light" for viewing bacterial colonies in soft agar. Methods Enzymol 2007; 423: 432– 435 [CrossRef] [PubMed]
    [Google Scholar]
  25. Storch KF, Rudolph J, Oesterhelt D. Car: a cytoplasmic sensor responsible for arginine chemotaxis in the archaeon Halobacterium salinarum. EMBO J 1999; 18: 1146– 1158 [CrossRef] [PubMed]
    [Google Scholar]
  26. Ditty JL, Parales RE. Protocols for the measurement of hydrocarbon chemotaxis in bacteria. In McGenity TJ, Timmis KN, Nogales B. (editors) Hydrocarbon and Lipid Microbiology Protocols Berlin: Springer-Verlag; 2017; pp. 7– 42
    [Google Scholar]
  27. Pham HT, Parkinson JS. Phenol sensing by Escherichia coli chemoreceptors: a nonclassical mechanism. J Bacteriol 2011; 193: 6597– 6604 [CrossRef] [PubMed]
    [Google Scholar]
  28. Plaggenborg R, Overhage J, Steinbüchel A, Priefert H. Functional analyses of genes involved in the metabolism of ferulic acid in Pseudomonas putida KT2440. Appl Microbiol Biotechnol 2003; 61: 528– 535 [CrossRef] [PubMed]
    [Google Scholar]
  29. Mohan K, Phale PS. Carbon source-dependent inducible metabolism of veratryl alcohol and ferulic acid in Pseudomonas putida CSV86. Appl Environ Microbiol 2017; 83: e03326-16 [CrossRef] [PubMed]
    [Google Scholar]
  30. Jiménez JI, Miñambres B, García JL, Díaz E. Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 2002; 4: 824– 841 [CrossRef] [PubMed]
    [Google Scholar]
  31. Calisti C, Ficca AG, Barghini P, Ruzzi M. Regulation of ferulic catabolic genes in Pseudomonas fluorescens BF13: involvement of a MarR family regulator. Appl Microbiol Biotechnol 2008; 80: 475– 483 [CrossRef] [PubMed]
    [Google Scholar]
  32. Parke D, Ornston LN. Hydroxycinnamate (hca) catabolic genes from Acinetobacter sp. strain ADP1 are repressed by HcaR and are induced by hydroxycinnamoyl-coenzyme A thioesters. Appl Environ Microbiol 2003; 69: 5398– 5409 [CrossRef] [PubMed]
    [Google Scholar]
  33. Hirakawa H, Schaefer AL, Greenberg EP, Harwood CS. Anaerobic p-coumarate degradation by Rhodopseudomonas palustris and identification of CouR, a MarR repressor protein that binds p-coumaroyl coenzyme A. J Bacteriol 2012; 194: 1960– 1967 [CrossRef] [PubMed]
    [Google Scholar]
  34. Otani H, Stogios PJ, Xu X, Nocek B, Li SN et al. The activity of CouR, a MarR family transcriptional regulator, is modulated through a novel molecular mechanism. Nucleic Acids Res 2016; 44: 595– 607 [CrossRef] [PubMed]
    [Google Scholar]
  35. Sarand I, Osterberg S, Holmqvist S, Holmfeldt P, Skärfstad E et al. Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of three polar localized Aer-like proteins of Pseudomonas putida. Environ Microbiol 2008; 10: 1320– 1334 [CrossRef] [PubMed]
    [Google Scholar]
  36. Ni B, Huang Z, Fan Z, Jiang CY, Liu SJ. Comamonas testosteroni uses a chemoreceptor for tricarboxylic acid cycle intermediates to trigger chemotactic responses towards aromatic compounds. Mol Microbiol 2013; 90: 813– 823 [CrossRef] [PubMed]
    [Google Scholar]
  37. Ni B, Huang Z, Wu YF, Fan Z, Jiang CY et al. A novel chemoreceptor MCP2983 from Comamonas testosteroni specifically binds to cis-aconitate and triggers chemotaxis towards diverse organic compounds. Appl Microbiol Biotechnol 2015; 99: 2773– 2781 [CrossRef] [PubMed]
    [Google Scholar]
  38. Rabinovitch-Deere CA, Parales RE. Three types of taxis used in the response of Acidovorax sp. strain JS42 to 2-nitrotoluene. Appl Environ Microbiol 2012; 78: 2306– 2315 [CrossRef] [PubMed]
    [Google Scholar]
  39. Grimm AC, Harwood CS. NahY, a catabolic plasmid-encoded receptor required for chemotaxis of Pseudomonas putida to the aromatic hydrocarbon naphthalene. J Bacteriol 1999; 181: 3310– 3316 [PubMed]
    [Google Scholar]
  40. Iwaki H, Muraki T, Ishihara S, Hasegawa Y, Rankin KN et al. Characterization of a pseudomonad 2-nitrobenzoate nitroreductase and its catabolic pathway-associated 2-hydroxylaminobenzoate mutase and a chemoreceptor involved in 2-nitrobenzoate chemotaxis. J Bacteriol 2007; 189: 3502– 3514 [CrossRef] [PubMed]
    [Google Scholar]
  41. Fernández M, Matilla MA, Ortega Á, Krell T. Metabolic value chemoattractants are preferentially recognized at broad ligand range chemoreceptor of Pseudomonas putida KT2440. Front Microbiol 2017; 8: 990 [CrossRef] [PubMed]
    [Google Scholar]
  42. Nichols NN, Harwood CS. Repression of 4-hydroxybenzoate transport and degradation by benzoate: a new layer of regulatory control in the Pseudomonas putida beta-ketoadipate pathway. J Bacteriol 1995; 177: 7033– 7040 [CrossRef] [PubMed]
    [Google Scholar]
  43. Parales RE, Luu RA, Chen GY, Liu X, Wu V et al. Pseudomonas putida F1 has multiple chemoreceptors with overlapping specificity for organic acids. Microbiology 2013; 159: 1086– 1096 [CrossRef] [PubMed]
    [Google Scholar]
  44. Greer-Phillips SE, Alexandre G, Taylor BL, Zhulin IB. Aer and Tsr guide Escherichia coli in spatial gradients of oxidizable substrates. Microbiology 2003; 149: 2661– 2667 [CrossRef] [PubMed]
    [Google Scholar]
  45. White AK, Metcalf WW. The htx and ptx operons of Pseudomonas stutzeri WM88 are new members of the Pho regulon. J Bacteriol 2004; 186: 5876– 5882 [CrossRef] [PubMed]
    [Google Scholar]
  46. Finette BA, Subramanian V, Gibson DT. Isolation and characterization of Pseudomonas putida PpF1 mutants defective in the toluene dioxygenase enzyme system. J Bacteriol 1984; 160: 1003– 1009 [PubMed]
    [Google Scholar]
  47. Gibson DT, Hensley M, Yoshioka H, Mabry TJ. Formation of (+)-cis-2,3-dihydroxy-1-methylcyclohexa-4,6-diene from toluene by Pseudomonas putida. Biochemistry 1970; 9: 1626– 1630 [PubMed] [Crossref]
    [Google Scholar]
  48. Liu X, Wood PL, Parales JV, Parales RE. Chemotaxis to pyrimidines and identification of a cytosine chemoreceptor in Pseudomonas putida. J Bacteriol 2009; 191: 2909– 2916 [CrossRef] [PubMed]
    [Google Scholar]
  49. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 1998; 212: 77– 86 [CrossRef] [PubMed]
    [Google Scholar]
  50. Figurski DH, Helinski DR. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 1979; 76: 1648– 1652 [CrossRef]
    [Google Scholar]
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