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Inoculation of PAH-degrading strains of Fusarium solani and Arthrobacter oxydans in rhizospheric sand and soil microcosms: microbial interactions and PAH dissipation

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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.

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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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  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, 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

    Article  PubMed  CAS  Google Scholar 

  • Kallimanis A, Labutti KM, Lapidus A (2011) Complete genome sequence of Arthrobacter phenanthrenivorans type strain (Sphe3). Stand Genomic Sci 4:123–130

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  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 indigenous microflora. Appl Environ Microbiol 64:2853–2858

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Liste HH, Prutz I (2006) Plant performance, dioxygenase-expressing rhizosphere bacteria, and biodegradation of weathered hydrocarbons in contaminated soil. Chemosphere 62:1411–1420

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wilcke W (2000) Polycyclic aromatic hydrocarbons (PAHs) in soils: a review. J Plant Nutr Soil Sci 163:229–248

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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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.

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Authors and Affiliations

  1. Université de Lorraine, CNRS, LIMOS, UMR 7137, BP 70239, 54506, Vandoeuvre-lès-Nancy, Cedex, France

    Cécile Thion, Aurélie Cébron, Thierry Beguiristain & Corinne Leyval

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  1. Cécile Thion
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  2. Aurélie Cébron
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  3. Thierry Beguiristain
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  4. Corinne Leyval
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Correspondence to Corinne Leyval.

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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

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