Skip to main content
Log in

Differential composition of bacterial communities as influenced by phenanthrene and dibenzo[a,h]anthracene in the rhizosphere of ryegrass (Lolium perenne L.)

  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

Bioremediation technologies of Polycyclic Aromatic Hydrocarbons (PAH) are often limited by the recalcitrance to biodegradation of high molecular weight (HMW) PAH. Rhizosphere is known to increase the biodegradation of PAH but little is known about the biodegradability of these HMW compounds by␣rhizosphere bacteria. This study compared the effects of a 3 and a 5-ring PAH, phenanthrene (PHE) and␣dibenzo[a,h]anthracene (dBA) respectively, on the composition of bacterial community, the bacterial density and the biodegradation activity. Compartmentalized devices were designed to harvest three consecutive sections of the rhizosphere. Rhizosphere and non-rhizosphere compartments were filled with PHE or dBA spiked or unspiked sand and inoculated with a soil bacterial inoculum. Different bacterial communities and degradation values were found 5 weeks after spiking with PHE (41–76% biodegradation) and dBA (12–51% biodegradation). In sections closer to the root surface, bacterial populations differed as a function of the distance to roots and the PAH added, whereas in further rhizosphere sections, communities were closer to those of the non-planted treatments. Biodegradation of PHE was also a function of the distance to roots, and decreased from 76 to 42% within 9 mm from the roots. However, biodegradation of dBA was significantly higher in the middle section (3–6 mm from roots) than the others. Rhizosphere degradation of PAH varies with the nature of the PAH, and C fluxes from roots could limit the degradation of dBA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson TA, Coats JR, (1994) Bioremediation throught Rhizosphere Technology. Anderson, TA and Coats JR, New York

    Google Scholar 

  • Binet P, Portal JM, Leyval C, (2000a) Dissipation of 3–6-ring polycyclic aromatic hydrocarbons in the rhizosphere of ryegrass Soil Biol. Biochem. 32: 2011–2017

    Article  CAS  Google Scholar 

  • Binet P, Portal JM, Leyval C, (2000) Fate of polycyclic aromatic hydrocarbons (PAH) in the rhizosphere and mycorrhizosphere of ryegrass Plant Soil 227: 207–213

    Article  CAS  Google Scholar 

  • Bogan BW, Schoenike B, Lamar RT, Cullen D, (1996) Manganese peroxidase mRNA and enzyme activity levels during bioremediation of polycyclic aromatic hydrocarbon-contaminated soil Phanerochaete chrysosporium Appl. Environ. Microbiol. 62: 2381–2386

    PubMed  CAS  Google Scholar 

  • Boochan S, Britz ML, Stanley GA, (2000) Degradation and mineralisation of height–molecular-weight polycyclic aromatic hydrocarbons by defined fungal–bacterial coculture Appl. Environ. Microbiol. 66: 1007–1019

    Article  PubMed  Google Scholar 

  • Corgié SC, Joner E, Leyval C, (2003) Rhizospheric degradation of phenanthrene is a function of proximity to roots Plant Soil 275: 143–150

    Article  Google Scholar 

  • Corgié SC, Beguiristain T, Leyval C, (2004) Spatial distribution of bacterial communities and phenanthrene (PHE) degradation in the rhizosphere of Lolium perenne L Appl. Environ. Microbiol. 70: 3552–3557

    Article  PubMed  CAS  Google Scholar 

  • Dabestani R, Ivanov I, (1999) A compilation of physical, spectroscopic and photohysical properties of polycyclic aromatic hydrocarbons Photochem. Photobiol. 70: 10–34

    Article  CAS  Google Scholar 

  • Déziel E, Paquette G, Villemur R, Lépine F, Bisaillon J-G, (1996) Biosurfactant production by a soil Pseudomonas strain growing on polycyclic aromatic hydrocarbons Appl. Environ. Microbiol. 62: 1908–1912

    Google Scholar 

  • Eschenbach A, Mahro B & Weinberg R (2000) Formation, long-term stability, and fate of non extractable 14C-PAH residues in contaminated soils. In: Wise DL, Trantolo DJ, Cichon EJ, Inyang HI & Stottmeister U (Eds) Remediation Engineering of Contaminated Soils (pp. 427–446). New York: Marcel Dekker, New York

  • Günther T, Dornberger U, Fritsche W, (1996) Effects of Ryegrass on biodegradation of hydrocarbons in soil Chemosphere 33: 203–215

    Article  PubMed  Google Scholar 

  • Heuer H, Hartung K, Wieland G, Kramer I, Smalla K, (1999) Polynucleotide probes that target a hypervariable region of 16S rRNA genes to identify bacterial isolates corresponding to bands of community fingerprints Appl. Environ. Microbiol. 65: 1045–1049

    PubMed  CAS  Google Scholar 

  • Höflich G, Günther T, (2000) Effect of plant-rhizosphere microorganism-associations on the degradation of polycyclic aromatic hydrocarbons in soil Die Dodenkultur 51: 91–97

    Google Scholar 

  • Joner EJ, Leyval C, (2003) Rhizosphere gradients of polycyclic aromatic hydrocarbon (PAH) dissipation in two industrial soils and the impact of arbuscular mycorrhiza Environ. Sci. Technol. 37: 2371–2375

    Article  PubMed  CAS  Google Scholar 

  • Joner EJ, Johansen A, Loibner AP, de la Cruz MA, Szolar OH, Portal JM, Leyval C, (2001) Rhizosphere effects on microbial community structure and dissipation and toxicity of polycyclic aromatic hydrocarbons (PAHs) in spiked soil Environm. Sci. Technol. 35: 2773–2777

    Article  PubMed  CAS  Google Scholar 

  • Joner EJ, Corgie SC, Amellal N, Leyval C, (2002) Nutritional constraints to degradation of polycyclic aromatic hydrocarbons in a simulated rhizosphere Soil Biol. Biochem. 34: 859–864

    Article  CAS  Google Scholar 

  • Juhasz AL, Britz ML, Stanley GA, (1997) Degradation of benzo(a)pyrene, dibenzo(a,h)anthracene and coronene by Burkholderia cepacia Water Sci. Technol. 36: 45–51

    Article  CAS  Google Scholar 

  • Juhasz AL, Naidu R, (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo(a)pyrene Int. Biodeter. Biodegr. 45: 57–88

    Article  CAS  Google Scholar 

  • Kanaly RA, Bartha R, Watanabe K, Harayama S, (2000) rapid mineralization of benzo(a)pyrene by a microbial consortium growing on diesel fuel Appl. Environ. Microbiol. 66: 4205–4211

    Article  PubMed  CAS  Google Scholar 

  • Kotterman MJJ, Vis EH, Field JA, (1998) Successive mineralization and detoxification of benzo(a)pyrene by the white rot fungus Bjerkandera sp. strain BOS55 and indegenous microflora Appl. Environ. Microbiol. 64: 2853–2858

    PubMed  CAS  Google Scholar 

  • Leyval C, Binet P, (1998) Effect of polyaromatic hydrocarbons in soil on arbuscular mycorrhizal plants J. Environ. Qual. 27: 402–407

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Löser C, Seidel H, Zehnsdorf A, Hoffmann P, (2000) Improvement of the bioavaibility of hydrocarbons by applying nonionic surfactants during the microbial remediation of a sandy soil Acta Biotechnol. 20: 99–118

    Article  Google Scholar 

  • Macek T, Mackova M, Kas J, (2000) Exploitation of plants for the removal of organics in environmental remediation Biotechnol. Adv. 18: 23–24

    Article  PubMed  CAS  Google Scholar 

  • Maier RM, Soberon-Chavez G, (2000) Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications Appl. Microbiol. Biotechnol. 54: 625–633

    Article  PubMed  CAS  Google Scholar 

  • Marschner B, (1999) Sorption of polycyclic aromatic hydrocarbons (PAH) and polychlorinated biphenyls (PCB) in soil J. Plant nutr. Soil Sci. 162: 1–14

    Article  CAS  Google Scholar 

  • Marschner P, Baumann K, (2003) Changes in bacterial community structure induced by mycorrhizal colonisation in spilt-root maize Plant Soil 251: 279–289

    Article  CAS  Google Scholar 

  • Means JC, (1980) Sorption of polynuclear aromatic hydrocarbons by sediment and soils Environ. Sci. Technol. 14: 1524–1528

    Article  CAS  Google Scholar 

  • Pickard MA, Roman R, Tinoco R, Vazquez-Duhalt R, (1999) Polycyclic aromatic hydrocarbon metabolism by white rot fungi and oxidation by Coriolopsis gallica UAMH 8260 laccase Appl. Environ. Microbiol. 65: 3805–3809

    PubMed  CAS  Google Scholar 

  • Rovira AD, (1969) Plant root exudates Bot. Rev. 35: 35–57

    CAS  Google Scholar 

  • Schneider J, Grosser R, Jayasimhulu K, Xue W, Warshawsky D, (1996) Degradation of pyrene, benz[a]anthracene, and benzo[a]pyrene by Mycobacterium sp. strain RJGII-135, isolated from a former coal gasification site Appl. Environ. Microbiol. 62: 13–19

    PubMed  CAS  Google Scholar 

  • Siciliano SD, Germida JJ, Banks K, Greer CW, (2003) Changes in microbial community composition and function during polyaromatic hydrocarbon phytoremediation field trial Appl. Environ. Microbiol. 69: 483–489

    Article  PubMed  CAS  Google Scholar 

  • Tang J, Carroquino J, Robertson BK, MA, (1998) Combined effect of sequestration and bioremediation in reducing the bioavaibility of polycyclic aromatic hydrocarbons in soil Environ. Sci. Technol. 32: 3586–3590

  • Walton BT, Hoylman AM, Perez MM, Anderson TA, Johnson TR, Guthrie EA & Christman RF (1994) Rhizosphere microbial communities as a plant defense against toxic substances in soils. Anderson, TA and Coats JR, 1155 Sixteenth St NW/Washington/DC 20036

  • Warembourg FR, Estelrich HD, (2000) Towards a better understanding of carbon flow in the rhizosphere: a time-dependent approach using carbon-14 Biol. and Fert. Soils 30: 528–534

    Article  CAS  Google Scholar 

  • Weissenfels WD, Klewer HJ, Langhoff J, (1992) Adsorption of polycyclic aromatic hydrocarbons (PAHs) by soil particles: influence on biodegradability and biotoxicity Appl. Microbiol. Biotechnol. 36: 689–696

    Article  PubMed  CAS  Google Scholar 

  • Wickle W, (2000) Polycyclic aromatic hydrocarbons (PAHs) in soil – a review J. Plant nutr. Soil Sci. 163: 229–248

    Article  Google Scholar 

  • Yoshitomi KJ, Shann JR, (2001) Corn (Zea mays L.) root exudates and their impact on 14C-pyrene mineralization Soil Biology and Biochemistry 33: 1769–1776

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Leyval.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Corgié, S., Beguiristain, T. & Leyval, C. Differential composition of bacterial communities as influenced by phenanthrene and dibenzo[a,h]anthracene in the rhizosphere of ryegrass (Lolium perenne L.). Biodegradation 17, 511–521 (2006). https://doi.org/10.1007/s10532-005-9022-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-005-9022-x

Keywords

Navigation