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Plant exudates promote PCB degradation by a rhodococcal rhizobacteria

  • Environmental biotechnology
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Abstract

Rhodococcus erythropolis U23A is a polychlorinated biphenyl (PCB)-degrading bacterium isolated from the rhizosphere of plants grown on a PCB-contaminated soil. Strain U23A bphA exhibited 99% identity with bphA1 of Rhodococcus globerulus P6. We grew Arabidopsis thaliana in a hydroponic axenic system, collected, and concentrated the plant secondary metabolite-containing root exudates. Strain U23A exhibited a chemotactic response toward these root exudates. In a root colonizing assay, the number of cells of strain U23A associated to the plant roots (5.7 × 105 CFU g−1) was greater than the number remaining in the surrounding sand (4.5 × 104 CFU g−1). Furthermore, the exudates could support the growth of strain U23A. In a resting cell suspension assay, cells grown in a minimal medium containing Arabidopsis root exudates as sole growth substrate were able to metabolize 2,3,4′- and 2,3′,4-trichlorobiphenyl. However, no significant degradation of any of congeners was observed for control cells grown on Luria–Bertani medium. Although strain U23A was unable to grow on any of the flavonoids identified in root exudates, biphenyl-induced cells metabolized flavanone, one of the major root exudate components. In addition, when used as co-substrate with sodium acetate, flavanone was as efficient as biphenyl to induce the biphenyl catabolic pathway of strain U23A. Together, these data provide supporting evidence that some rhodococci can live in soil in close association with plant roots and that root exudates can support their growth and trigger their PCB-degrading ability. This suggests that, like the flagellated Gram-negative bacteria, non-flagellated rhodococci may also play a key role in the degradation of persistent pollutants.

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References

  • Abramowicz DA (1995) Aerobic and anaerobic PCB biodegradation in the environment. Environ Health Persp 103:97–99

    CAS  Google Scholar 

  • Arai H, Kosono S, Taguchi K, Maeda M, Song E, Fuji F, Chung SY, Kudo T (1998) Two sets of biphenyl and PCB degradation genes on a linear plasmid in Rhodococcus erythropolis TA421. J Ferment Bioeng 86:595–599

    Article  CAS  Google Scholar 

  • Asturias JA, Moore E, Yakimov MM, Klatte S, Timmis KN (1994) Reclassification of the polychlorinated biphenyl-degraders Acinetobacter sp. strain P6 and Corynebacterium sp. strain MB1 as Rhodococcus globerulus. Syst Appl Microbiol 17:226–231

    Article  CAS  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32

    Article  CAS  Google Scholar 

  • Barriault D, Plante MM, Sylvestre M (2002) Family shuffling of a targeted bphA region to engineer biphenyl dioxygenase. J Bacteriol 184:3794–3800

    Article  CAS  Google Scholar 

  • Barriault D, Lépine F, Mohammadi M, Milot S, Leberre N, Sylvestre M (2004) Revisiting the regiospecificity of Burkholderia xenovorans LB400 biphenyl dioxygenase toward 2,2′-dichlorobiphenyl and 2,3,2′,3′-tetrachlorobiphenyl. J Biol Chem 279:47489–47496

    Article  CAS  Google Scholar 

  • Bedard DL, Unterman R, Bopp LH, Brennan MJ, Haberl ML, Johnson C (1986) Rapid assay for screening and characterizing microorganisms for the ability to degrade polychlorinated biphenyls. Appl Environ Microbiol 51:761–768

    CAS  Google Scholar 

  • Borja J, Taleon DM, Auresenia J, Gallardo S (2005) Polychlorinated biphenyls and their biodegradation. Proc Biochem 40:1999–2013

    Article  CAS  Google Scholar 

  • Brazil GM, Kenefick L, Callanan M, Haro A, Delorenzo V, Dowling DN, Ogara F (1995) Construction of a rhizosphere pseudomonad with potential to degrade polychlorinated-biphenyls and detection of bph gene-expression in the rhizosphere. Appl Environ Microbiol 61:1946–1952

    CAS  Google Scholar 

  • Chebrou H, Hurtubise Y, Barriault D, Sylvestre M (1999) Heterologous expression and characterization of the purified oxygenase component of Rhodococcus globerulus P6 biphenyl dioxygenase and of chimeras derived from it. J Bacteriol 181:4805–4811

    CAS  Google Scholar 

  • Chekol T, Vough LR, Chaney RL (2004) Phytoremediation of polychlorinated biphenyl-contaminated soils: the rhizosphere effect. Environ Int 30:799–804

    Article  CAS  Google Scholar 

  • Chung SY, Maeda M, Song E, Horikoshi K, Kudo T (1994) A gram-positive polychlorinated biphenyl-degrading bacterium, Rhodococcus erytrhopolis strain TA421, isolated from a termite ecosystem. Biosci Biotechnol Biochem 58:2111–2113

    Article  CAS  Google Scholar 

  • Daar AS, Thorsteinsdottir H, Martin DK, Smith AC, Nast S, Singer PA (2002) Top ten biotechnologies for improving health in developing countries. Nat Genet 32:229–232

    Article  CAS  Google Scholar 

  • de Lorenzo V, Pérez-Martin J (1996) Regulatory noise in prokaryotic promoters: how bacteria learn to respond to novel environmental signals. Mol Microbiol 19:1177–1184

    Article  Google Scholar 

  • Dercova K, Tandlich R, Brezna B (2003) Application of terpenes as possible inducers of biodegradation of PCBs. Fresen Environ Bull 12:286–290

    CAS  Google Scholar 

  • Déziel E, Comeau Y, Villemur R (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183:1195–1204

    Article  Google Scholar 

  • Donnelly PK, Hegde RS, Fletcher JS (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28:981–988

    Article  Google Scholar 

  • Edwards U, Rogall T, Blocker H, Emde M, Bottger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853

    Article  CAS  Google Scholar 

  • Fava F, Bertin L (1999) Use of exogenous specialised bacteria in the biological detoxification of a dump site-polychlorobiphenyl-contaminated soil in slurry phase conditions. Biotechnol Bioeng 64:240–249

    Article  CAS  Google Scholar 

  • Field JA, Sierra-Alvarez R (2008) Microbial degradation of chlorinated dioxins. Chemosphere 71:1005–1018

    Article  CAS  Google Scholar 

  • Fletcher JS, Hegde RS (1995) Release of phenols by perennial plant-roots and their potential importance in bioremediation. Chemosphere 31:3009–3016

    Article  CAS  Google Scholar 

  • Francis I, Holsters M, Vereecke D (2010) The Gram-positive side of plant–microbe interactions. Environ Microbiol 12:1–12

    Article  CAS  Google Scholar 

  • Gilbert ES, Crowley DE (1997) Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl Environ Microbiol 63:1933–1938

    CAS  Google Scholar 

  • Gordillo F, Chavez FP, Jerez CA (2007) Motility and chemotaxis of Pseudomonas sp B4 towards polychlorobiphenyls and chlorobenzoates. FEMS Microbiol Ecol 60:322–328

    Article  CAS  Google Scholar 

  • Hernandez BS, Koh SC, Chial M, Focht DD (1997) Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil. Biodegradation 8:153–158

    Article  CAS  Google Scholar 

  • Hurtubise Y, Barriault D, Sylvestre M (1996) Characterization of active recombinant his-tagged oxygenase component of Comamonas testosteroni B-356 biphenyl dioxygenase. J Biol Chem 271:8152–8156

    Article  CAS  Google Scholar 

  • Hurtubise Y, Barriault D, Sylvestre M (1998) Involvement of the terminal oxygenase beta subunit in the biphenyl dioxygenase reactivity pattern toward chlorobiphenyls. J Bacteriol 180:5828–5835

    CAS  Google Scholar 

  • Imbeault NY, Powlowski JB, Colbert CL, Bolin JT, Eltis LD (2000) Steady-state kinetic characterization and crystallization of a polychlorinated biphenyl-transforming dioxygenase. J Biol Chem 275:12430–12437

    Article  CAS  Google Scholar 

  • Iwasaki T, Miyauchi K, Masai E, Fukuda M (2006) Multiple-subunit genes of the aromatic-ring-hydroxylating dioxygenase play an active role in biphenyl and polychlorinated biphenyl degradation in Rhodococcus sp strain RHA1. Appl Environ Microbiol 72:5396–5402

    Article  CAS  Google Scholar 

  • Jarrell KF, McBride MJ (2008) The surprisingly diverse ways that prokaryotes move. Nature Rev Microbiol 6:466–476

    Article  CAS  Google Scholar 

  • Kearns DB (2010) A field guide to bacterial swarming motility. Nature Rev Microbiol 8:634–644

    Article  CAS  Google Scholar 

  • Kim BH, Oh ET, So JS, Ahn Y, Koh SC (2003) Plant terpene-induced expression of multiple aromatic ring hydroxylation oxygenase genes in Rhodococcus sp strain T104. J Microbiol 41:349–352

    CAS  Google Scholar 

  • L’Abbée JB, Tu Y, Barriault D, Sylvestre M (2011) Insight into the metabolism of 1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane (DDT) by biphenyl dioxygenases. Arch Biochem Biophys 516:35–44

    Article  Google Scholar 

  • Leigh MB, Fletcher JS, Fu XO, Schmitz FJ (2002) Root turnover: an important source of microbial substrates in rhizosphere remediation of recalcitrant contaminants. Environ Sci Technol 36:1579–1583

    Article  CAS  Google Scholar 

  • Leigh MB, Prouzova P, Mackova M, Macek T, Nagle DP, Fletcher JS (2006) Polychlorinated biphenyl (PCB)-degrading bacteria associated with trees in a PCB-contaminated site. Appl Environ Microbiol 72:2331–2342

    Article  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Ann Rev Microbiol 63:541–556

    Article  CAS  Google Scholar 

  • Luo WS, D’Angelo EM, Coyne MS (2007) Plant secondary metabolites, biphenyl, and hydroxypropyl-beta-cyclodextrin effects on aerobic polychlorinated biphenyl removal and microbial community structure in soils. Soil Biol Biochem 39:735–743

    Article  CAS  Google Scholar 

  • Masak J, Cejkova A, Jirku V, Kotrba D, Hron P, Siglova M (2005) Colonization of surfaces by phenolic compounds utilizing microorganisms. Environ Int 31:197–200

    Article  CAS  Google Scholar 

  • Massé R, Messier F, Ayotte C, Lévesque M-F, Sylvestre M (1989) A Comprehensive gas chromatographic/Mass spectrometric analysis of 4-chlorobiphenyl bacterial degradation products. Biomed Environ Mass 18:27–47

    Article  Google Scholar 

  • McKay DB, Prucha M, Reineke W, Timmis KN, Pieper DH (2003) Substrate specificity and expression of three 2,3-dihydroxybiphenyl 1,2-dioxygenases from Rhodococcus globerulus strain P6. J Bacteriol 185:2944–2951

    Article  CAS  Google Scholar 

  • Miya RK, Firestone MK (2001) Enhanced phenanthrene biodegradation in soil by slender oat root exudates and root debris. J Environ Qual 30:1911–1918

    Article  CAS  Google Scholar 

  • Mohammadi M, Viger JF, Kumar P, Barriault D, Bolin JT, Sylvestre M (2011) Retuning Rieske-type oxygenases to expand substrate range. J Biol Chem 286:27612–27621

    Article  CAS  Google Scholar 

  • Murray TS, Kazmierczak BI (2008) Pseudomonas aeruginosa exhibits sliding motility in the absence of type IV pili and flagella. J Bacteriol 190:2700–2708

    Article  CAS  Google Scholar 

  • Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant–microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153

    Article  CAS  Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Ann Rev Microbiol 54:49–79

    Article  Google Scholar 

  • Pieper DH (2005) Aerobic degradation of polychlorinated biphenyls. Appl Microbiol Biot 67:170–191

    Article  CAS  Google Scholar 

  • Rosenberg M (2006) Microbial adhesion to hydrocarbons: twenty-five years of doing MATH. FEMS Microbiol Lett 262:129–134

    Article  CAS  Google Scholar 

  • Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Sanchez-Contreras M, Martin M, Villacieros M, O’Gara F, Bonilla I, Rivilla R (2002) Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J Bacteriol 184:1587–1596

    Article  CAS  Google Scholar 

  • Scher FM, Ziegle JS, Kloepper JW (1984) A method for assessing the root-colonizing capacity of bacteria on maize. Can J Microbiol 30:151–157

    Article  Google Scholar 

  • Seeger M, Gonzalez M, Camara B, Munoz L, Ponce E, Mejias L, Mascayano C, Vasquez Y, Sepulveda-Boza S (2003) Biotransformation of natural and synthetic isoflavonoids by two recombinant microbial enzymes. Appl Environ Microbiol 69:5045–5050

    Article  CAS  Google Scholar 

  • Seo J, Kang SI, Kim M, Han J, Hur HG (2011) Flavonoids biotransformation by bacterial non-heme dioxygenases, biphenyl and naphthalene dioxygenase. Appl Microbiol Biot 91:219–228

    Article  CAS  Google Scholar 

  • Seto M, Ida M, Okita N, Hatta T, Masai E, Fukuda M (1996) Catabolic potential of multiple PCB transformation systems in Rhodococcus sp strain RHA1. Biotechnol Lett 18:1305–1308

    Article  CAS  Google Scholar 

  • Shaw LJ, Morris P, Hooker JE (2006) Perception and modification of plant flavonoids signals by rhizosphere microorganisms. Environ Microbiol 8:1867–1880

    Article  CAS  Google Scholar 

  • Shindo K, Kagiyama Y, Nakamura R, Hara A, Ikenaga H, Furukawa K, Misawa N (2003) Enzymatic synthesis of novel antioxidant flavonoids by Escherichia coli cells expressing modified metabolic genes involved in biphenyl catabolism. J Mol Catal B-Enzym 23:9–16

    Article  CAS  Google Scholar 

  • Shindo K, Osawa A, Nakamura R, Kagiyama Y, Sakuda S, Shizuri Y, Furukawa K, Misawa N (2004) Conversion from arenes having a benzene ring to those having a picolinic acid by simple growing cell reactions using Escherichia coli that expressed the six bacterial genes involved in biphenyl catabolism. J Am Chem Soc 126:15042–15043

    Article  CAS  Google Scholar 

  • Singer AC, Crowley DE, Thompson IP (2003) Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol 21:123–130

    Article  CAS  Google Scholar 

  • Sylvestre M (1980) Isolation method for bacterial isolates capable of growth on p-chlorobiphenyl. Appl Environ Microbiol 39:1223–1224

    CAS  Google Scholar 

  • Sylvestre M, Toussaint JP (2011) Engineering microbial enzymes and plants to promote PCB degradation in soil: current state of knowledge. In: Koukkou AI (ed) Microbial bioremediation of non-metals current research. Caister Academic, Norfolk, pp 177–196

    Google Scholar 

  • Sylvestre M, Macek T, Mackova M (2009) Transgenic plants to improve rhizoremediation of polychlorinated biphenyls (PCBs). Curr Opin Biotechnol 20:242–247

    Article  CAS  Google Scholar 

  • Trivedi P, Pandey A, Sa TM (2007) Chromate reducing and plant growth promoting activies of psychrotrophic Rhodococcus erythropolis MtCC 7905. J Basic Microb 47:513–517

    Article  CAS  Google Scholar 

  • Van Aken B, Correa PA, Schnoor JL (2010) Phytoremediation of polychlorinated biphenyls: new trends and promises. Environ Sci Technol 44:2767–2776

    Article  Google Scholar 

  • Vasilyeva GK, Strijakova ER (2007) Bioremediation of soils and sediments contaminated by polychlorinated biphenyls. Microbiology 76:639–653

    Article  CAS  Google Scholar 

  • Vézina J, Barriault D, Sylvestre M (2007) Family shuffling of soil DNA to change the regiospecificity of Burkholderia xenovorans LB400 biphenyl dioxygenase. J Bacteriol 189:779–788

    Article  Google Scholar 

  • Villacieros M, Whelan C, Mackova M, Molgaard J, Sanchez-Contreras M, Lloret J, de Carcer DA, Oruezabal RI, Bolanos L, Macek T, Karlson U, Dowling DN, Martin M, Rivilla R (2005) Polychlorinated biphenyl rhizoremediation by Pseudomonas fluorescens F113 derivatives, using a Sinorhizobium meliloti nod system to drive bph gene expression. Appl Environ Microbiol 71:2687–2694

    Article  CAS  Google Scholar 

  • Warren R, Hsiao WWL, Kudo H, Myhre M, Dosanjh M, Petrescu A, Kobayashi H, Shimizu S, Miyauchi K, Masai E, Yang G, Stott JM, Schein JE, Shin H, Khattra J, Smailus D, Butterfield YS, Siddiqui A, Holt R, Marra MA, Jones SJM, Mohn WW, Brinkman FSL, Fukuda M, Davies J, Eltis LD (2004) Functional characterization of a catabolic plasmid from polychlorinated-biphenyl-degrading Rhodococcus sp strain RHA1. J Bacteriol 186:7783–7795

    Article  CAS  Google Scholar 

  • Yang XQ, Sun Y, Qian SJ (2004) Biodegradation of seven polychlorinated biphenyls by a newly isolated aerobic bacterium (Rhodococcus sp R04). J Ind Microbiol Biotechnol 31:415–420

    Article  CAS  Google Scholar 

  • Yang X, Liu X, Song L, Xie F, Zhang G, Qian S (2007) Characterization and functional analysis of a novel gene cluster involved in biphenyl degradation in Rhodococcus sp strain R04. J Appl Microbiol 103:2214–2224

    Article  CAS  Google Scholar 

  • Yun Q, Lin Z, Xin T (2009) Cometabolism and immobilized degradation of monochlorobenzoate by Rhodococcus erythropolis. Afr J Microbiol Res 3:482–486

    CAS  Google Scholar 

  • Zhang GQ, Yang XQ, Xie FH, Chao YP, Qian SJ (2009) Cometabolic degradation of mono-chloro benzoic acids by Rhodococcus sp R04 grown on organic carbon sources. World J Microbiol Biotechnol 25:1169–1174

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by grant STPSC 356996-07 from the Natural Sciences and Engineering Research Council of Canada. We thank Prof. David Dowling, Institute of Technology, Carlow, Ireland, who generously provided Pseudomonas fluorescens F113. We thank Prof. Martina Mackova, Prague Institute of Chemical Technology, Prague, Czech Republic, for providing the PCB-contaminated soil used in this investigation. We also thank Inspec-Sol Inc., Montreal, Quebec, Canada for providing an in-kind contribution to this work.

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  1. Jean-Patrick Toussaint

    Present address: Fondation David Suzuki, 50 rue Sainte-Catherine Ouest, Montréal, QC, H2X 3 V4, Canada

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  1. Institut National de la Recherche Scientifique, INRS-Institut Armand-Frappier, 531 Boul. des Prairies, Laval, QC, H7V 1B7, Canada

    Jean-Patrick Toussaint, Thi Thanh My Pham, Diane Barriault & Michel Sylvestre

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Correspondence to Michel Sylvestre.

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Toussaint, JP., Pham, T.T.M., Barriault, D. et al. Plant exudates promote PCB degradation by a rhodococcal rhizobacteria. Appl Microbiol Biotechnol 95, 1589–1603 (2012). https://doi.org/10.1007/s00253-011-3824-z

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