Abstract
Very little is known about the influence of bacterial-fungal ecological interactions on polycyclic aromatic hydrocarbon (PAH) dissipation in soils. Fusarium solani MM1 and Arthrobacter oxydans MsHM11 can dissipate PAHs in vitro. We investigated their interactions and their effect on the dissipation of three PAHs—phenanthrene (PHE), pyrene (PYR) and dibenz(a,h)anthracene (DBA)—in planted microcosms, in sterile sand or non-sterile soil. In sterile sand microcosms planted with alfalfa, the two microbes survived and grew, without any significant effect of co-inoculation. Co-inoculation led to the dissipation of 46 % of PHE after 21 days. In soil microcosms, whether planted with alfalfa or not, both strains persisted throughout the 46 days of the experiment, without any effect of co-inoculation or of alfalfa, as assessed by real-time PCR targeting taxon-level indicators, i.e. Actinobacteria 16S rDNA and the intergenic transcribed spacer specific to the genus Fusarium. The microbial community was analyzed by temporal temperature gradient electrophoresis and real-time PCR targeting bacterial and fungal rDNA and PAH-ring hydroxylating dioxygenase genes. These communities were modified by PAH pollution, which selected PAH-degrading bacteria, by the presence of alfalfa and, concerning the bacterial community, by inoculation. PHE and PYR concentrations significantly decreased (91 and 46 %, respectively) whatever the treatment, but DBA concentration significantly decreased (30 %) in planted and co-inoculated microcosms only.
Similar content being viewed by others
References
Abd-Elsalam KA, Aly IN, Abdel-Satar MA, Khalil MS, Verreet JA (2003) PCR identification of Fusarium genus based on nuclear ribosomal-DNA sequence data. Afr J Biotechnol 2:96–103
Adesina MF, Grosch R, Lembke A, Vatchev TD, Smalla K (2009) In vitro antagonists of Rhizoctonia solani tested on lettuce: rhizosphere competition, biocontrol efficiency and rhizosphere microbial community response. FEMS Microbiol Ecol 69:62–74
Andersson BE, Welinder L, Olsson PA, Olsson S, Henrysson T (2000) Growth of inoculated white-rot fungi and their interactions with the bacterial community in soil contaminated with polycyclic aromatic hydrocarbons, as measured by phospholipid fatty acids. Bioresour Technol 73:29–36
Biache C, Mansuy-Huault L, Faure P, Munier-Lamy C, Leyval C (2008) Effects of thermal desorption on the composition of two coking plant soils: impact on solvent extractable organic compounds and metal bioavailability. Environ Pollut 156:671–677
Boonchan S, Britz ML, Stanley GA (2000) Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal-bacterial cocultures. Appl Environ Microbiol 66:1007–1019
Buée M, De Boer W, Martin F, Overbeek L, Jurkevitch E (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212
Byss M, Elhottov D, Tříska J, Baldrian P (2008) Fungal bioremediation of the creosote-contaminated soil: influence of Pleurotus ostreatus and Irpex lacteus on polycyclic aromatic hydrocarbons removal and soil microbial community composition in the laboratory-scale study. Chemosphere 73:1518–1523
Cébron A, Norini MP, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDalpha) genes from gram positive and gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148–159
Cébron A, Beguiristain Faure P, Norini MP, Masfaraud JF, Leyval C (2009) Influence of vegetation on the in situ bacterial community and polycyclic aromatic hydrocarbon (PAH) degraders in aged PAH-contaminated or thermal-desorption-treated soil. Appl Environ Microbiol 75:6322–6330
Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 4:331–338
Chiapusio G, Pujol S, Toussaint M, Badot P, Binet P (2007) Phenanthrene toxicity and dissipation in rhizosphere of grassland plants (Lolium perenne L. and Trifolium pratense L.) in three spiked soils. Plant Soil 294:103–112
Coppotelli BM, Ibarrolaza A, Del Panno MT, Morelli IS (2008) Effects of the inoculant strain Sphingomonas paucimobilis 20006FA on soil bacterial community and biodegradation in phenanthrene-contaminated soil. Microb Ecol 55:173–183
Corgié SC, Beguiristain T, Leyval C (2004) Spatial distribution of bacterial communities and phenanthrene degradation in the rhizosphere of Lolium perenne L. Appl Environ Microbiol 70:3552–3557
Criquet S, Joner E, Leglize P, Leyval C (2000) Anthracene and mycorrhiza affect the activity of oxidoreductases in the roots and the rhizosphere of lucerne (Medicago sativa L.). Biotechnol Lett 22:1733–1737
D’Annibale A, Ricci M, Leonardi V, Quaratino D, Mincione E, Petruccioli M (2005) Degradation of aromatic hydrocarbons by white-rot fungi in a historically contaminated soil. Biotechnol Bioeng 90:723–731
de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811
Felske A, Akkermans ADL, De Vos WM (1998) Quantification of 16S rRNAs in complex bacterial communities by multiple competitive reverse transcription-PCR in temperature gradient gel electrophoresis fingerprints. Appl Environ Microbiol 64:4581–4587
Garbeva G, Termorshuizen AJ, Hol G, Kowalchuk GA, de Boer W (2011) Fungistasis and general soil biostasis: a new synthesis. Soil Biol Biochem 43:469–477
Gramss G, Kirsche B, Voigt KD, Günther T, Fritsche W (1999) Conversion rates of five polycyclic aromatic hydrocarbons in liquid cultures of fifty-eight fungi and the concomitant production of oxidative enzymes. Mycol Res 103:1009–1018
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15
Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241
Hong JW, Park JY, Gadd GM (2010) Pyrene degradation and copper and zinc uptake by Fusarium solani and Hypocrea lixii isolated from petrol station soil. J Appl Microbiol 108:2030–2040
Joner E, Leyval C (2001) Influence of arbuscular mycorrhiza on clover and ryegrass grown together in a soil spiked with polycyclic aromatic hydrocarbons. Mycorrhiza 10:155–159
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
Joner EJ, Hirmann D, Szolar OH, Todorovic D, Leyval C, Loibner AP (2004) Priming effects on PAH degradation and ecotoxicity during a phytoremediation experiment. Environ Pollut 128:429–435
Kallimanis A, Labutti KM, Lapidus A (2011) Complete genome sequence of Arthrobacter phenanthrenivorans type strain (Sphe3). Stand Genomic Sci 4:123–130
Kang H, Hwang SY, Kim YM, Kim E, Kim YS, Kim SK, Kim SW, Cerniglia CE, Shuttleworth KL, Zylstra GJ (2003) Degradation of phenanthrene and naphthalene by a Burkholderia species strain. Can J Microbiol 49:139–144
Kim SJ, Kweon O, Jones RC, Edmondson RD, Cerniglia CE (2008) Genomic analysis of polycyclic aromatic hydrocarbon degradation in Mycobacterium vanbaalenii PYR-1. Biodegrad 19:859–881
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 indigenous microflora. Appl Environ Microbiol 64:2853–2858
Lang E, Nerud F, Zadrazil F (1998) Production of ligninolytic enzymes by Pleurotus sp. and Dichomitus squalens in soil and lignocellulose substrate as influenced by soil microorganisms. FEMS Microbiol Lett 167:239–244
Liste HH, Prutz I (2006) Plant performance, dioxygenase-expressing rhizosphere bacteria, and biodegradation of weathered hydrocarbons in contaminated soil. Chemosphere 62:1411–1420
Louvel B, Cébron A, Leyval C (2011) Root exudates affect phenanthrene biodegradation, bacterial community and functional gene expression in sand microcosms. Inter Biodeter Biodegrad 65:947–953
Marek ET, Schardl CL, Smith DA (1989) Molecular transformation of Fusarium solani with an antibiotic resistance marker having no fungal DNA homology. Curr Genet 15:421–428
Masoud W, Takamiya M, Vogensen FK, Lillevang S, Al-Soud WA, Sørensen SJ, Jakobsen M (2011) Characterization of bacterial populations in Danish raw milk cheeses made with different starter cultures by denaturating gradient gel electrophoresis and pyrosequencing. Int Dairy J 21:142–148
Muratova AY, Turkovskaya OV, Hübner T, Kuschk P (2003) studies of the efficacy of alfalfa and reed in the phytoremediation of hydrocarbon-polluted soil. Appl Biochem Microbiol 39:599–605
Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955
Phillips LA, Germida JJ, Farrell RE, Greer CW (2008) Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol Biochem 40:3054–3064
Potin O, Veignie E, Rafin C (2004) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by Cladosporium sphaerospermum isolated from an aged PAH contaminated soil. FEMS Microbiol Ecol 51:71–78
Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361
Redon PO, Beguiristain T, Leyval C (2009) Differential effects of AM fungal isolates on Medicago truncatula growth and metal uptake in a multimetallic (Cd, Zn, Pb) contaminated agricultural soil. Mycorrhiza 19:187–195
Schwartz E, Trinh SV, Scow KM (2000) Measuring growth of a phenanthrene-degrading bacterial inoculum in soil with a quantitative competitive polymerase chain reaction method. FEMS Microbiol Ecol 34:1–7
Silva IS, Santos EC, Menezes CR, Faria AF, Franciscon E, Grossman M, Durrant LR (2009) Bioremediation of a polyaromatic hydrocarbon contaminated soil by native soil microbiota and bioaugmentation with isolated microbial consortia. Bioresour Technol 100:4669–4675
Smit E, Leeflang P, Glandorf B, van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65:2614–2621
Thion C, Cébron A, Béguiristain T, Leyval C (2012a) PAH biotransformation and sorption by Fusarium solani and Arthrobacter oxydans isolated from a polluted soil in axenic cultures and mixed co-cultures. Int Biodeter Biodegrad 68:28–35
Thion C, Cébron A, Béguiristain T, Leyval C (2012b) Long-term in situ dynamics of the fungal communities in a multi-contaminated soil are mainly driven by plants. FEMS Microbiol Ecol 82:169–181
Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104:927–936
van Elsas JD, Duarte GF, Keijzer-Wolters A, Smit E (2000) Analysis of the dynamics of fungal communities in soil via fungal-specific PCR of soil DNA followed by denaturing gradient gel electrophoresis. J Microbiol Methods 43:133–151
van Veen JA, van Overbeek LS, van Elsas JD (1997) Fate and activity of microorganisms introduced into soil. Microbiol Mol Biol Rev 61:121–135
Verdin A, Sahraoui AL-H, Durand R (2004) Degradation of benzo[a]pyrene by mitosporic fungi and extracellular oxidative enzymes. Int Biodeter Biodegrad 53(2):65–70
Wilcke W (2000) Polycyclic aromatic hydrocarbons (PAHs) in soils: a review. J Plant Nutr Soil Sci 163:229–248
Zhou XB, Cébron A, Béguiristain T, Leyval C (2009) Water and phosphorus content affect PAH dissipation in spiked soil planted with mycorrhizal alfalfa and tall fescue. Chemosphere 77(6):709–713
Acknowledgments
The authors gratefully acknowledge the ANR program (MULTIPOLSITE, ANR-2008-CESA-010) and GISFI (Groupement d’Intérêt Scientifique sur les Friches Industrielles, www.gisfi.fr) for financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Thion, C., Cébron, A., Beguiristain, T. et al. Inoculation of PAH-degrading strains of Fusarium solani and Arthrobacter oxydans in rhizospheric sand and soil microcosms: microbial interactions and PAH dissipation. Biodegradation 24, 569–581 (2013). https://doi.org/10.1007/s10532-013-9628-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-013-9628-3