Environmental Science and Pollution Research

, Volume 24, Issue 20, pp 16735–16750 | Cite as

Impact of metal stress on the production of secondary metabolites in Pteris vittata L. and associated rhizosphere bacterial communities

  • Hoang Nam Pham
  • Serge Michalet
  • Josselin Bodillis
  • Tien Dat Nguyen
  • Thi Kieu Oanh Nguyen
  • Thi Phuong Quynh Le
  • Mohamed Haddad
  • Sylvie Nazaret
  • Marie-Geneviève Dijoux-Franca
Research Article


Plants adapt to metal stress by modifying their metabolism including the production of secondary metabolites in plant tissues. Such changes may impact the diversity and functions of plant associated microbial communities. Our study aimed to evaluate the influence of metals on the secondary metabolism of plants and the indirect impact on rhizosphere bacterial communities. We then compared the secondary metabolites of the hyperaccumulator Pteris vittata L. collected from a contaminated mining site to a non-contaminated site in Vietnam and identified the discriminant metabolites. Our data showed a significant increase in chlorogenic acid derivatives and A-type procyanidin in plant roots at the contaminated site. We hypothesized that the intensive production of these compounds could be part of the antioxidant defense mechanism in response to metals. In parallel, the structure and diversity of bulk soil and rhizosphere communities was studied using high-throughput sequencing. The results showed strong differences in bacterial composition, characterized by the dominance of Proteobacteria and Nitrospira in the contaminated bulk soil, and the enrichment of some potential human pathogens, i.e., Acinetobacter, Mycobacterium, and Cupriavidus in P. vittata’s rhizosphere at the mining site. Overall, metal pollution modified the production of P. vittata secondary metabolites and altered the diversity and structure of bacterial communities. Further investigations are needed to understand whether the plant recruits specific bacteria to adapt to metal stress.


Bacterial communities Metal stress Pteris vittata Rhizosphere Secondary metabolites 



Ultrahigh-performance liquid chromatography with diode array detection coupled to electrospray ionization and quadrupole time-of-flight mass spectrometry




Electrospray ionization


Tandem mass spectrometry


Electrospray ionization tandem mass spectrometry


High-resolution mass spectrometry


Proton nuclear magnetic resonance


Retention time


Solid phase extraction


Soil under P. vittata polluted


Bulk soil polluted


Soil under Dicranopteris linearis polluted


Soil under P. vittata control


Honest significant difference


Principal component analysis


Analysis of variance


Colony forming unit


Quantitative real-time polymerase chain reaction


Operational taxonomic unit


Denaturing gradient gel electrophoresis





Hoang Nam Pham wish to gratefully thank the Vietnam Ministry of Education and Training, the University of Sciences and Technologies of Hanoi, and team “Environmental resistance and bacterial efflux,” UMR 5557 CNRS Microbial Ecology, for the financial support. We thank the platforms CESN (Centre d’Etudes des Substances Naturelles) and PARMIC (Plateau d’Analyse du Risque MICrobiologique, UMR Ecologie Microbienne, Université Lyon1) for the equipment facilities, and Institut of Marine Biochemistry (Vietnam Academy of Science and Technology, Hanoi) is also acknowledged for providing valuable assessment during the development of this subject.

Supplementary material

11356_2017_9167_MOESM1_ESM.docx (157 kb)
Fig. S1 Typical UHPLC/DAD chromatogram at 280 nm of P. vittata root extracts. PVP: From plants grown on contaminated soil (Ha Thuong); PVC: From plants grown on non-polluted soil (USTH) (DOCX 157 kb).
11356_2017_9167_MOESM2_ESM.docx (183 kb)
Fig. S2 Typical UHPLC/DAD chromatogram at 280 nm of P. vittata stems extracts. PVP: From plants grown on contaminated soil (Ha Thuong); PVC: From plants grown on non-polluted soil (USTH) (DOCX 182 kb).
11356_2017_9167_MOESM3_ESM.docx (186 kb)
Fig. S3 Typical UHPLC/DAD chromatogram at 280 nm of P. vittata leaves extracts. PVP: From plants grown on contaminated soil (Ha Thuong); PVC: From plants grown on non-polluted soil (USTH) (DOCX 185 kb).
11356_2017_9167_MOESM4_ESM.docx (12 kb)
Table S1 (DOCX 11 kb).


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Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Hoang Nam Pham
    • 1
    • 2
  • Serge Michalet
    • 1
  • Josselin Bodillis
    • 1
  • Tien Dat Nguyen
    • 3
  • Thi Kieu Oanh Nguyen
    • 2
  • Thi Phuong Quynh Le
    • 4
  • Mohamed Haddad
    • 5
  • Sylvie Nazaret
    • 1
  • Marie-Geneviève Dijoux-Franca
    • 1
  1. 1.UMR 5557, Ecologie Microbienne, CNRS, INRA, VetagroSup, UCBLUniversité de LyonVilleurbanneFrance
  2. 2.University of Science and Technology of Hanoi, Vietnam Academy of Science and TechnologyHanoiVietnam
  3. 3.Institute of Marine BiochemistryVietnam Academy of Science and TechnologyHanoiVietnam
  4. 4.Institute of Natural Products ChemistryVietnam Academy of Science and TechnologyHanoiVietnam
  5. 5.UMR 152 Pharma-DEVUniversité de Toulouse, IRD, UPSToulouseFrance

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