Skip to main content
SpringerLink
Log in

Influence of Miscanthus × giganteus and Trifolium repens L. on microflora and PAH-degrading bacteria in contaminated technosol

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Rhizodegradation is the breakdown of organic contaminants such as polycyclic aromatic hydrocarbons (PAHs) using plants and rhizospheric microorganisms. The influence of two phytoremediating plants, Miscanthus × giganteus (M × G) and Trifolium repens L., was studied on a PAH-contaminated technosol composed of soil and sediments. More specifically, microbial density and diversity were studied along with the density of the population of PAH-degrading bacteria.

Methods

M × G and white clover were tested in mono- and co-culture on the technosol in a mesocosm over 263 days (life cycle of M × G until its senescence). At the beginning and the end of the phytoremediation experiment, microbial density was measured by real-time PCR, targeting bacteria (16S rDNA), fungi (18S rDNA), and PAH-degrading bacteria (PAH-RHDα GP). Bacterial and fungal diversity were determined by metagenomic analysis.

Results

The M × G monoculture appeared to increase bacterial diversity compared to non-planted technosol, in contrast to other planting patterns, while fungal diversity appeared to decrease in the presence of any of the plants. Overall, the plants increased the bacterial density in the technosol, while only white clover and the co-culture increased the fungal density, with the latter having a greater impact. Concerning the degrading bacteria, only the co-culture stimulated the PAH-degrading bacterial population. This is remarkable for the PAH rhizodegradation.

Conclusion

Even though the co-culture seemed to decrease the microbial diversity in the technosol, this condition was the most interesting with respect to the increase of the bacterial and fungal density as well as the enhancement of the PAH-degrading bacteria in the technosol.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Availability of data and material

Not applicable.

Code availability

Not applicable.

References

  • Abdel-Shafy HI, Mansour MSM (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25:107–123. https://doi.org/10.1016/j.ejpe.2015.03.011

    Article  Google Scholar 

  • AFNOR (2015) NF EN ISO 11268–1. Soil quality—effects of pollutants on earthworms—part 1: determination of acute toxicity to Eisenia fetida

  • AIDA (2008) Circulaire du 04/07/08 relative à la procédure concernant la gestion des sédiments lors de travaux ou d’opérations impliquant des dragages ou curages maritimes et fluviaux|AIDA. https://aida.ineris.fr/consultation_document/7177. Accessed 6 Mar 2020

  • Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192. https://doi.org/10.1016/S0038-0717(03)00179-2

    Article  CAS  Google Scholar 

  • Bidar G, Garçon G, Pruvot C et al (2007) Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147:546–553. https://doi.org/10.1016/j.envpol.2006.10.013

    Article  CAS  Google Scholar 

  • Bourgeois E, Dequiedt S, Lelièvre M et al (2015) Positive effect of the Miscanthus bioenergy crop on microbial diversity in wastewater-contaminated soil. Environ Chem Lett 13:495–501. https://doi.org/10.1007/s10311-015-0531-5

    Article  CAS  Google Scholar 

  • Cébron A, Norini M-P, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDα) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148–159. https://doi.org/10.1016/j.mimet.2008.01.009

    Article  CAS  Google Scholar 

  • Chen Y, Tian W, Shao Y et al (2020) Miscanthus cultivation shapes rhizosphere microbial community structure and function as assessed by Illumina MiSeq sequencing combined with PICRUSt and FUNGUIld analyses. Arch Microbiol 202:1157–1171. https://doi.org/10.1007/s00203-020-01830-1

    Article  CAS  Google Scholar 

  • Darmendrail D (2000) Fonds géochimique naturel–État des connaissances à l’échelle nationale. INRA/BRGM. BRGM/RP-50158-FR, juin 2000. Étude réalisée dans le cadre des actions de Service public du BRGM 99-F-269

  • Gao Y, Miao C, Xia J et al (2012) Plant diversity reduces the effect of multiple heavy metal pollution on soil enzyme activities and microbial community structure. Front Environ Sci Eng 6:213–223. https://doi.org/10.1007/s11783-011-0345-z

    Article  CAS  Google Scholar 

  • Gerhardt KE, Huang X-D, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30

    Article  CAS  Google Scholar 

  • Lange M, Eisenhauer N, Sierra CA et al (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6:6707. https://doi.org/10.1038/ncomms7707

    Article  CAS  Google Scholar 

  • Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. https://doi.org/10.1016/j.soilbio.2008.05.021

    Article  CAS  Google Scholar 

  • Laval-Gilly P, Henry S, Mazziotti M et al (2017) Miscanthus x giganteus composition in metals and potassium after culture on polluted soil and its use as biofuel. Bioenergy Res 10:846–852. https://doi.org/10.1007/s12155-017-9846-3

    Article  CAS  Google Scholar 

  • Lewandowski I, Heinz A (2003) Delayed harvest of miscanthus—influences on biomass quantity and quality and environmental impacts of energy production. Eur J Agron 19:45–63. https://doi.org/10.1016/S1161-0301(02)00018-7

    Article  Google Scholar 

  • Li S, Wu F (2018) Diversity and co-occurrence patterns of soil bacterial and fungal communities in seven intercropping systems. Front Microbiol 9:1521. https://doi.org/10.3389/fmicb.2018.01521

    Article  Google Scholar 

  • Lowther WL (1975) Pelleting materials for oversown clover. New Zeal J Exp Agr 3:121–125. https://doi.org/10.1080/03015521.1975.10425787

    Article  Google Scholar 

  • Maliszewska-Kordybach B (1999) Sources, concentrations, fate and effects of polycyclic aromatic hydrocarbons (PAHs) in the environment. Part A: PAHs in air. Pol J Environ Stud 8:131–136

    CAS  Google Scholar 

  • Martin-Laurent F, Philippot L, Hallet S et al (2001) DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl Environ Microbiol 67:2354–2359

    Article  CAS  Google Scholar 

  • Mazziotti M (2017) Impact des exsudats racinaires de Miscanthus x giganteus sur les microorganismes impliqués dans la bioremédiation d’un sol contaminé au benzo(a)anthracène. Université de Lorraine

  • Mazziotti M, Henry S, Laval-Gilly P et al (2018) Comparison of two bacterial DNA extraction methods from non-polluted and polluted soils. Folia Microbiol 63:85–92. https://doi.org/10.1007/s12223-017-0530-y

    Article  CAS  Google Scholar 

  • Meng L, Qiao M, Arp HPH (2011) Phytoremediation efficiency of a PAH-contaminated industrial soil using ryegrass, white clover, and celery as mono- and mixed cultures. J Soils Sediments 11:482–490. https://doi.org/10.1007/s11368-010-0319-y

    Article  CAS  Google Scholar 

  • Mitchell RJ, Campbell CD, Chapman SJ, Cameron CM (2010) The ecological engineering impact of a single tree species on the soil microbial community: tree impacts on the soil microbial community. J Ecol 98:50–61. https://doi.org/10.1111/j.1365-2745.2009.01601.x

    Article  CAS  Google Scholar 

  • Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    Article  CAS  Google Scholar 

  • Neukirchen D, Himken M, Lammel J et al (1999) Spatial and temporal distribution of the root system and root nutrient content of an established Miscanthus crop. Eur J Agron 11:301–309

    Article  Google Scholar 

  • Newbould P, Rangeley A (1984) Effect of lime, phosphorus and mycorrhizal fungi on growth, nodulation and nitrogen fixation by white clover (Trifolium repens) grown in UK hill soils. Plant Soil 76:105–114. https://doi.org/10.1007/BF02205571

    Article  CAS  Google Scholar 

  • Nsanganwimana F, Pourrut B, Mench M, Douay F (2014) Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services. A Review J Env Manage 143:123–134. https://doi.org/10.1016/j.jenvman.2014.04.027

    Article  CAS  Google Scholar 

  • Schneider A (2015) (ed) Les légumineuses pour des systèmes agricoles et alimentaires durables. Éditions Quae, Versailles

  • Smit E, Leeflang P, Glandorf B et al (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

    Article  CAS  Google Scholar 

  • Sterckeman T, Ouvrard S, Leglize P (2011) Phytoremédiation des sols. Les techniques de l’ingénieur

  • Techer D, D’Innocenzo M, Laval-Gilly P et al (2012) Assessment of Miscanthus × giganteus secondary root metabolites for the biostimulation of PAH-utilizing soil bacteria. Appl Soil Ecol 62:142–146. https://doi.org/10.1016/j.apsoil.2012.06.009

    Article  Google Scholar 

  • Técher D, Laval-Gilly P, Henry S et al (2011) Contribution of Miscanthus x giganteus root exudates to the biostimulation of PAH degradation: an in vitro study. Sci Total Environ 409:4489–4495. https://doi.org/10.1016/j.scitotenv.2011.06.049

    Article  CAS  Google Scholar 

  • Touzé S (2013) Procédé innovant de traitement de la fraction fine de sédiments pollués. Techniques de l’ingénieur

  • 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 

  • Wechtler L, Henry S, Falla J et al (2020) Polycyclic aromatic hydrocarbons (PAHs) dissipation from a contaminated technosol composed of dredged sediments with Miscanthus x giganteus and Trifolium repens L. in mono- and co-culture. J Soils Sediments. https://doi.org/10.1007/s11368-020-02648-6

  • Xu SY, Chen YX, Lin KF et al (2009) Removal of pyrene from contaminated soils by white clover. Pedosphere 19:265–272. https://doi.org/10.1016/S1002-0160(09)60117-X

    Article  CAS  Google Scholar 

  • Xu SY, Chen YX, Wu WX et al (2006) Enhanced dissipation of phenanthrene and pyrene in spiked soils by combined plants cultivation. Sci Total Environ 363:206–215. https://doi.org/10.1016/j.scitotenv.2005.05.030

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr Mélanie Mazziotti for the establishment of the standard range in real-time PCR. We gratefully thank Pascale and Marine Sauton (San Jose, California) for their English revision.

Funding

Financial support was received from “Communauté d’Agglomération Portes de France – Thionville,” “Communauté de Communes Cattenom et Environs,” and “Communauté de Communes du Pays Orne Moselle.”

Author information

Authors and Affiliations

  1. Université de Lorraine, INRAE, 54000, Nancy, LSE, France

    Laura Wechtler, Sonia Henry, Sandhya Malladi, Jaïro Falla-Angel & Philippe Laval-Gilly

  2. Université de Lorraine, IUT Thionville-Yutz, 57970, Yutz, France

    Antoine Bonnefoy

Authors
  1. Laura Wechtler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sonia Henry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sandhya Malladi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antoine Bonnefoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jaïro Falla-Angel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Philippe Laval-Gilly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Laura Wechtler or Philippe Laval-Gilly.

Ethics declarations

Human and animal rights

This research did not involve any human participants and/or animals.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Yuan Ge

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wechtler, L., Henry, S., Malladi, S. et al. Influence of Miscanthus × giganteus and Trifolium repens L. on microflora and PAH-degrading bacteria in contaminated technosol. J Soils Sediments 22, 208–217 (2022). https://doi.org/10.1007/s11368-021-03055-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-021-03055-1

Keywords

Search

Navigation