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Horizontal transfer of genetic determinants for degradation of phenol between the bacteria living in plant and its rhizosphere

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Abstract

Phenol and other monocyclic aromatic compounds (MACs) are highly water-soluble and volatile pollutants that plants are unable to completely degrade. Endophytic bacteria with MAC-degrading ability will facilitate phytoremediation, beneficial to plant survival in contaminated soil. Endophytic bacteria, strains FX1–FX3, and rhizosphere bacteria, strains FX0, FX4, and FX5, were isolated from the root tissue of a corn plant (Zea mays) and the corn rhizosphere near a chemical plant, respectively. The strains FX1–FX5 were able to grow on phenol and reduce phenol concentration, but the strain FX0 was unable to. The strains FX1, FX3, and FX4 were classified as Pseudomonas fluorescens and FX0, FX2, and FX5 as Burkholderia cepacia. The plasmids isolated from the strains FX1–FX5 were found to possess similar traits and to be loaded with a gene encoding the catechol 2, 3-dioxygenase (C23O), a key enzyme in the phenol degradation pathway. Alignment and phylogenetic analysis inferred that in situ horizontal transfer of the C23O gene might have occurred. The horizontal transfer of the C23O gene between endophytic and rhizosphere bacteria was proved by using conjugal matings experiment, in which the transconjugants were found to acquire the plasmid with the C23O gene, able to grow on phenol and degrade phenol.

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References

  • Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–588

    Article  CAS  PubMed  Google Scholar 

  • Bastos AE, Moon DH, Rossi A, Trevors JT, Tsai SM (2000) Salt-tolerant phenol-degrading microorganisms isolated from Amazonian soil samples. Arch Microbiol 174:346–52

    Article  CAS  PubMed  Google Scholar 

  • Burken JG, Schnoor JL (1999) Distribution and volatilization of organic compounds following uptake by hybrid poplar trees. Int J Phytoremediat 1:139–151

    Article  CAS  Google Scholar 

  • Cerdan P, Rekik M, Harayama S (1995) Substrate specificity differences between two catechol 2,3-dioxygenases encoded by the TOL and NAH plasmids from Pseudomonas putida. Eur J Biochem 229:113–118

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed WS, Ibrahim MK, Abu-Shady M, El-Beih F, Ohmura N, Saiki H, Ando A (2003) Isolation and identification of a novel strain of the genus Ochrobactrum with phenol-degrading activity. J Biosci Bioeng 96:310–312

    Article  CAS  PubMed  Google Scholar 

  • Eltis LD, Bolin JT (1996) Evolutionary relationships among extradiol dioxygenases. J Bacteriol 178:5930–5937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Entezari MH, Petrier C (2005) A combination of ultrasound and oxidative enzyme: sono-enzyme degradation of phenols in a mixture. Ultrason Sonochem 12:283–288

    Article  CAS  PubMed  Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284

    Article  CAS  PubMed  Google Scholar 

  • Fries MR, Forney LJ, Tiedje JM (1997) Phenol- and toluene-degrading microbial populations from an aquifer in which successful trichloroethene cometabolism occurred. Appl Environ Microbiol 63:1523–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • George PP, Andrew JD (2005) Enhanced biodegradation of phenol by a microbial consortium in a solid–liquid two phase partitioning bioreactor. Biodegradation 16:329–339

    Article  CAS  Google Scholar 

  • Hearn EM, Dennis JJ, Gray MR, Foght JM (2003) Identification and characterization of the emhABC efflux system for polycyclic aromatic hydrocarbons in Pseudomonas fluorescens cLP6a. J Bacteriol 185:6233–6240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt JG, Krieg NRP, Sneath HA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams & Wilkins, Baltimore, MD

    Google Scholar 

  • Hübner TM, Tischer S, Tanneberg H, Kuschk P (2000) Influence of Phenol and Phenanthrene on the growth of Phalaris arundinacea and Phragmites australis. Int J Phytoremediat 2:331–342

    Article  Google Scholar 

  • Isken S, de Bont JAM (1996) Active efflux of toluene in a solvent resistant bacterium. J Bacteriol 178:6056–6058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang HL, Tay ST, Maszenan AM, Tay JH (2006) Physiological traits of bacterial strains isolated from phenol-degrading aerobic granules. FEMS Microbiol Ecol 57:182–191

    Article  CAS  PubMed  Google Scholar 

  • Kado CI, Liu ST (1981) Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145:1365–1373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelator in heavy metal contaminated land remediation. Chemosphere 41:197–207

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of basesubstitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescen. J Lab Clin Med 44:301–307

    CAS  PubMed  Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant-Microb Interact 17:6–15

    Article  CAS  Google Scholar 

  • Kukor JJ, Olsen RH (1996) Catechol 2, 3-dioxygenases functional in oxygen-limited hypoxic environments. Appl Environ Microbiol 62:1728–1740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Burken JG (2003) TCE diffusion to the atmosphere in phytoremediation applications. Environ Sci Technol 37:2534–2539

    Article  CAS  PubMed  Google Scholar 

  • Mahamuni NN, Pandit AB (2005) Effect of additives on ultrasonic degradation of phenol. Ultrason Sonochem 13:165–174

    Article  PubMed  CAS  Google Scholar 

  • Mars BE, Kingma J, Kaschabek SR, Reineke W, Janssen DB (1999) Conversion of 3-chlorocatechol by various catechol 2,3-dioxygenases and sequence analysis of the chlorocatechol dioxygenase region of Pseudomonas putida GJ31. J Bacteriol 181:1309–1318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin-Laurent F, Philippot L, Hallet S, Chaussod R, Germon JC, Soulas G, Catroux G (2001) DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl Environ Microbiol 67:2354–2359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann G, Teras R, Monson L, Kivisaar M, Schauer F, Heipieper HJ (2004) Simultaneous degradation of atrazine and phenol by Pseudomonas sp. strain ADP: effects of toxicity and adaptation. Appl Environ Microbiol 70:1907–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh JM, Kang E, Min KR, Kim CK, Kim YC, Lim JY, Lee KS, Min KH, Kim Y (1997) Structure of catechol 2, 3-dioxygenase gene encoded in TOM plasmid of Pseudomonas putida G4. Biochem Biophys Res Commun 234:578–581

    Article  CAS  PubMed  Google Scholar 

  • Okuta A, Ohnishi K, Harayama S (2004) Construction of chimeric catechol 2, 3-dioxygenase exhibiting improved activity against the suicide inhibitor 4-methylcatechol. Appl Environ Microbiol 70:1804–1810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polz MF, Cavanaugh CM (1998) Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64:3724–3730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Sayler GS, Hooper SW, Layton AC, King JMH (1990) Catabolic plasmids of environmental and ecological significance. Microb Ecol 19:1–20

    Article  CAS  PubMed  Google Scholar 

  • Sharma A, Kachroo D, Kumar R (2002) Time dependent influx and efflux of phenol by immobilized microbial consortium. Environ Monit Assess 76:195–211

    Article  CAS  PubMed  Google Scholar 

  • Shields MS, Montgomery SO, Cuskey SM, Chapman PJ, Pritchard PH (1991) Mutants of Pseudomonas cepacia G4 defective in catabolism of aromatic compounds and trichloroethylene. Appl Environ Microbiol 57:1935–1941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shields MS, Reagin MJ (1992) Selection of a Pseudomonas cepacia strain constitutive for the degradation of trichloroethylene. Appl Environ Microbiol 58:3977–3983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shields MS, Reagin MJ, Gerger RR, Campbell R, Somerville C (1995) TOM, a new aromatic degradative plasmid from Burkholderia (Pseudomonas) cepacia G4. Appl Environ Microbiol 61:1352–1356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MR (1990) The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation 1:191–206

    Article  CAS  PubMed  Google Scholar 

  • Stuart-Keil KG, Hohnstock AM, Drees KP, Herrick JB, Madsen EL (1998) Plasmids responsible for horizontal transfer of naphtalene catabolism genes between bacteria at a coal-contaminated site are homologous to pDTG1 from pseudomonas putida NCIB 9816-4. App Environ Microbiol 64:3633–3640

    Article  CAS  Google Scholar 

  • Taghavi S, Barac T, Greenberg B, Borremans B, Vangronsveld J, van der Lelie D (2005) Horizontal gene transfer to endogenous endophytic bacteria from poplar improves phytoremediation of toluene. Appl Environ Microbiol 71:8500–8505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Schie MP, Young LY (1998) Isolation and characterization of phenol-degrading denitrifying bacteria. Appl Environ Microbiol 64:1997–2438

    Article  Google Scholar 

  • Viggiani A, Siani L, Notomista E, Birolo L, Pucci P, Donato AD (2004) The role of the conserved residues his-246, his-199, and tyr-255 in the catalysis of catechol 2,3-dioxygenase from Pseudomonas stutzeri OX1. J Biol Chem 279:48630–48639

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K, Teramoto M, Futamata H, Harayama S (1998) Molecular detection, isolation, and physiological characterization of functionally dominant phenol-degrading bacteria in activated sludge. Appl Environ Microbiol 64:4396–4402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weissburg WG, Barns SM, Pelletier DA, Lane DL (1991) 16S robosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  Google Scholar 

  • Yuan Y (2005) Determination of volatile phenol from water by using spectrophotometry assay. China Trop Med 115:558–559

    Google Scholar 

Download references

Acknowledgment

This work was supported by the Shanghai Municipal Science and Technology Commission (04DZ19304), the Shanghai Municipal Education Commission (05ZZ14), and the National Natural Science Foundation of China (30670445).

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Authors and Affiliations

  1. College of Life and Environment Sciences, Shanghai Normal University, Shanghai, 200234, People’s Republic of China

    Yujing Wang, Ming Xiao, Xiaolu Geng, Jiaying Liu & Jun Chen

  2. Biology Department, College of Life and Environment Sciences, Shanghai Normal University, Shanghai, 200234, People’s Republic of China

    Ming Xiao

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  1. Yujing Wang
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  2. Ming Xiao
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  3. Xiaolu Geng
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  4. Jiaying Liu
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Correspondence to Ming Xiao.

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Wang, Y., Xiao, M., Geng, X. et al. Horizontal transfer of genetic determinants for degradation of phenol between the bacteria living in plant and its rhizosphere. Appl Microbiol Biotechnol 77, 733–739 (2007). https://doi.org/10.1007/s00253-007-1187-2

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