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Polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates: their association with plant roots

  • Environmental Biotechnology
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Abstract

Five environmental mycobacterium isolates that degrade polycyclic aromatic hydrocarbons (PAHs) were associated with barley root surfaces after growth of the seedlings from inoculated seed. Mycobacterium cells were detected along the total root length for four of these isolates. These PAH-degrading mycobacterium strains had hydrophilic cell surfaces, whereas one strain, MCS, that was hydrophobic had reduced association along the root length with no cells being detected from the root tips. The root-tip-competent strain, KMS, was competitive for its root association in the presence of the root-colonizing pseudomonad, Pseudomonas putida KT2440. All mycobacterium strains utilized simple sugars (fructose, glucose) and the trisaccharide 6-kestose, present in barley root washes, for planktonic growth, but they differed in their potential for biofilm formation under in vitro conditions. Mineralization of pyrene by the KMS strain occurred when the components in the barley root wash were amended with labeled pyrene suggesting to us that mineralization could occur in plant rhizospheres containing such mycobacterium strains.

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References

  • Anderson AJ, Britt DW, Johnson J, Narsimhan G, Rodriguez A (2005) Physicochemical parameters influencing the formation of biofilms compared in mutant and wild type cells of Pseudomonas chlororaphis O6. Water Sci Technol 57:21–25

    Article  Google Scholar 

  • Anokhina TO, Kochetkov VV, Zelenkova NF, Balakshina VV, Boronin AM (2004) Biodegradation of phenanthrene by Pseudomonas bacteria bearing rhizospheric plasmids in model plant–microbial associations. Appl Biochem Microbiol 40:568–572

    Article  CAS  Google Scholar 

  • Bais HP, Fall R, Vivanco JM (2001) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319

    Article  CAS  Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001) Mucoid mutants of the biocontrol strain Pseudomonas fluorescens CHA0 show increased ability in biofilm formation on mycorrhizal and nonmycorrhizal carrot roots. Mol Plant–Microb Interact 14:255–260

    Article  CAS  Google Scholar 

  • Carter G, Wu M, Drummond DC, Bermudez LE (2003) Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J Med Microbiol 52:747–752

    Article  CAS  PubMed  Google Scholar 

  • Cerniglia CE (1993). Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 4:331–338

    Article  CAS  Google Scholar 

  • Chen YC, Banks MK, Schwab AP (2003) Pyrene degradation in the rhizosphere of tall fescue (Festuca arundinacea) and switchgrass (Panicum virgatum L.). Environ Sci Technol 37:5778–5782

    Article  CAS  PubMed  Google Scholar 

  • Chatterton NJ, Hardson PA (2003) Fructans in crested wheatgrass leaves. J Plant Physiol 160:843–849

    Article  CAS  PubMed  Google Scholar 

  • Cheung PY, Kinkle BK (2001) Mycobacterium diversity and pyrene mineralization in petroleum-contaminated soils. Appl Environ Microbiol 67:2222–2229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conn VM, Franco CM (2004) Analysis of the endophytic actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16S rRNA clones. Appl Environ Microbiol 70:1787–1794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunningham SD, Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol 110:715–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies GD, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298

    CAS  PubMed  Google Scholar 

  • Daane LL, Harjono I, Zylstra JG, Häggblom MM (2001) Isolation and characterization of polycyclic aromatic hydrocarbon-degrading bacteria associated with the rhizosphere of salt marsh plants. Appl Environ Microbiol 67:2683–2691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dean-Ross D, Cerniglia CE (1996) Degradation of pyrene by Mycobacterium flavescens. Appl Microbiol Biotechnol 46:307–312

    Article  CAS  PubMed  Google Scholar 

  • Derz K, Klinner U, Schuphan I, Stachebrandt E, Kroppenstedt RM (2004). Mycobacterium pyrenivorans sp. nov., a novel polycyclic-aromatic-hydrocarbon-degrading species. Int J Syst Evol Microbiol 54:2313–2317

    Article  CAS  PubMed  Google Scholar 

  • Djordjevic D, Wiedmann M, McLandsborough LA (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68:2950–2958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Espinosa-Urgel M, Salido A, Ramos JL (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182:2363–2369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferro AM, Sims RC, Bugbee B (1994) Hycrest crested wheatgrass accelerates the degradation of pentachlorophenol in soil. J Environ Qual 23:272–279

    Article  CAS  PubMed  Google Scholar 

  • Hall K, Miller CD, Sorensen DL, Anderson AJ, Sims RC (2005). Development of a catabolically significant genetic probe for polycyclic aromatic hydrocarbon-degrading mycobacteria in soil. Biodegradation 16:475–484

    Article  CAS  PubMed  Google Scholar 

  • Hall-Stoodley L, Lappin-Scott H (1998) Biofilm formation by the rapidly growing mycobacterial species Mycobacterium fortuitum. FEMS Microbiol Lett 168:77–84

    Article  CAS  PubMed  Google Scholar 

  • Harvey RG (1991) Polycyclic aromatic hydrocarbons chemistry and carcinogenicity. Cambridge Univ. Press, Cambridge, UK

    Google Scholar 

  • Heitkamp MA, Franklin W, Cerniglia CE (1988). Microbial metabolism of polycyclic aromatic hydrocarbons: isolation and characterization of a pyrene-degrading bacterium. Appl Environ Microbiol 54:2549–2555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henry GAF, Wallace RK (1993) The origin, distribution, and evolutionary significance of fructans. In: Suzuki M, Chatterton NJ (eds) Science and technology of fructans. CRC, Boca Raton, FL, pp 119–139

    Google Scholar 

  • Jackson RW, Preston GM, Rainey PB (2005) Genetic characterization of Pseudomonas fluorescens SBw25 rsp gene expression in the phylosphere and in vitro. J Bacteriol 187:8477–8488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James DW, Suslow TV, Steinback KE (1985). Relationship between rapid, firm adhesion and long-term colonization of roots by bacteria. Appl Environ Microbiol 50:392–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jana TK, Srivastava AK, Csery K, Arora DK (2000) Influence of growth and environmental conditions on cell surface hydrophobicity of Pseudomonas fluorescens in non-specific adhesion. Can J Microbiol 46:28–37

    Article  CAS  PubMed  Google Scholar 

  • Keuth S, Rehm HJ (1991) Biodegradation of phenanthrene by Arthrobacter polychromogenes isolated from contaminated soil. Appl Microbiol Biotechnol 34:804–808

    Article  CAS  Google Scholar 

  • Khan AA, Wang RF, Cao WW, Doerge DR, Wennerstrom D, Cerniglia CE. (2001) Molecular cloning, nucleotide sequence, and expression of genes encoding a polycyclic aromatic ring dioxygenase from Mycobacterium sp. Strain PYR-1. Appl Environ Microbiol 67:3577–3585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YB, Park KY, Chung Y, Oh KC, Buchanan BB (2004) Phytoremediation of anthracene contaminated soils by different plant species. J Plant Biol 47:174–178

    Article  CAS  Google Scholar 

  • Leys NM, Bastiaens L, Verstraete W, Springael D (2005) Influence of the carbon/nitrogen/phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil. Appl Microbiol Biotechnol 66:726–736

    Article  CAS  PubMed  Google Scholar 

  • Liste HH, Alexander M (2000) Plant-promoted pyrene degradation in soil. Chemosphere 40:7–10

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg BJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490

    Article  CAS  PubMed  Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10

    Article  CAS  Google Scholar 

  • Macrae S, Thomson JA, Van Staden J (1988) Colonization of tomato plants by two agrocin-producing strains of Agrobacterium tumefaciens. Appl Environ Microbiol 54:3133–3137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsollier L, Stinear T, Aubry J, AndreJPS, Robert R, Legras P, Manceau AL, Audrain C,Bourdon S, Kouakou H, Carbonnelle B (2004) Aquatic plants stimulate the growth of and biofilm formation by Mycobacterium ulcerans in axenic culture and harbor these bacteria in the environment. Appl Environ Microbiol 70:1097–1103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthysse AG, McMahan S (1998) Root colonization by Agrobacterium tumefaciens is reduced in cel, attB, attD, and attR mutants. Appl Environ Microbiol 64:2341–2345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menzie CA,. Potocki BB, Santodonato J (1992) Exposure to carcinogenic PAHs in the environment. Environ Sci Technol 26:1278–1284

    Article  CAS  Google Scholar 

  • Miller CD, Hall K, Liang YN, Nieman K, Sorensen D, Issa B, Anderson AJ, Sims RC (2004). Isolation and characterization of polycyclic aromatic hydrocarbon-degrading mycobacterium isolates from soil. Microb Ecol 48:230–238

    Article  CAS  PubMed  Google Scholar 

  • Miller CD, Child R, Hughes JE, Der JP, Sims RC, Anderson AJ (2006) Diversity of soil mycobacterium isolates from three sites that degrade polycyclic aromatic hydrocarbons. J Appl Microbiol. DOI https://doi.org/10.1111/j.1365-2672.2006.03202

  • Molina MA, Godoy P, Ramos-Gonzalez MI, Munoz N, Ramos JL, Espinosa-Urgel M (2005). Role of iron and the TonB system in colonization of corn seeds and roots by Pseudomonas putida KT2440. Environ Microbiol 7:443–449

    Article  CAS  PubMed  Google Scholar 

  • Moody JD, Freeman JP, Fu PP, Cerniglia CE (2004) Degradation of benzo[a]pyrene by Mycobacterium vanbaalenii PYR-1. Appl Environ Microbiol 70:340–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris CE, Monier JM (2003). The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41:429–453

    Article  CAS  PubMed  Google Scholar 

  • Nedunuri KV, Govindaraju RS, Banks MK, Schwab AP, Chen Z (2000) Evaluation of phytoremediation for field-scale degradation of total petroleum hydrocarbons. J Environ Eng 126:483–490

    Article  CAS  Google Scholar 

  • Patnaik P (1992) Hydrocarbon, aromatic. In: Patnaik P (ed) A comprehensive guide to the hazardous properties of chemical substances. Van Nostrand Reinhold, New York, NY, pp 425–445

    Google Scholar 

  • Paul EA, Clark FE (1989) Occurrences and distribution of soil organics. In: Paul EA, Clark FE (eds) Soil microbiology and biochemistry. Academic, San Diego, CA, pp 81–84

    Google Scholar 

  • Read DB, Bengough PJ, Gregory J, Crawford JW, Robinson D, Scrimgeour CM, Young IM, Zhang K, Zhang X (2003). Plant roots release phospholipids surfactants that modify the physical and chemical properties of soil. New Phytol 157:315–326

    Article  CAS  PubMed  Google Scholar 

  • Rentz JA, Alvarez PJ, Schnoor JL (2004) Repression of Pseudomonas putida phenanthrene-degrading activity by plant root extracts and exudates. Environ Microbiol 6:574–583

    Article  PubMed  Google Scholar 

  • Rose L, Kaufmann SH, Daugelat S (2004). Involvement of Mycobacterium smegmatis undecaprenyl phosphokinase in biofilm and smegma formation. Microbes Infect 6:965–971

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacteria N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant–Microb Interact 13:637–648

    Article  CAS  Google Scholar 

  • Tsao DT (2003) Overview of phytotechnologies. Adv Biochem Eng Biotechnol 78:4–50

    Google Scholar 

  • Van Loosdrecht MC, Lyklema J, Norde W, Schraa G, AJ Zehnder (1987) The role of bacterial cell wall hydrophobicity in adhesion. Appl Environ Microbiol 53:1893–1897

    Article  PubMed  PubMed Central  Google Scholar 

  • Varrot A, Leydier S, Pell G, Macdonald JM, Stick RV, Henrissat B, Gilbert HJ, Davies GJ (2005) Mycobacterium tuberculosis strains possess functional cellulases. J Biol Chem 280:20181–20184

    Article  CAS  PubMed  Google Scholar 

  • Walker TS, Bais HP, Deziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM (2004). Pseudomonas aeruginosa-plant root interactions. Pathgenicity, biofilm formation, and root exudation. Plant Physiol 134:320–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wick L, de Munain A, Springael D, Harms H (2002) Responses of Mycobacterium sp LB501T to the low bioavailability of solid anthracene. Appl Microbiol Biotechnol 58:378–385

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Utah State University, Logan, UT, 84322, USA

    R. Child, C. D. Miller & A. J. Anderson

  2. Department of Biological Engineering and Irrigation, Utah State University, Logan, UT, 84322, USA

    Y. Liang, G. Narasimham, R. C. Sims & D. Britt

  3. USDA Forage and Range Research Laboratory, Utah State University, Logan, UT, 84322, USA

    J. Chatterton & P. Harrison

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  1. R. Child
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  2. C. D. Miller
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Correspondence to A. J. Anderson.

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Child, R., Miller, C.D., Liang, Y. et al. Polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates: their association with plant roots. Appl Microbiol Biotechnol 75, 655–663 (2007). https://doi.org/10.1007/s00253-007-0840-0

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  • DOI: https://doi.org/10.1007/s00253-007-0840-0

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