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

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Abstract

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.

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Abbreviations

UHPLC-DAD-ESI/QTOF-MS:

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

UV:

Ultraviolet

ESI:

Electrospray ionization

MSMS:

Tandem mass spectrometry

ESI/MS2 :

Electrospray ionization tandem mass spectrometry

HRMS:

High-resolution mass spectrometry

1H-NMR:

Proton nuclear magnetic resonance

RT:

Retention time

SPE:

Solid phase extraction

PVP:

Soil under P. vittata polluted

BSP:

Bulk soil polluted

DLP:

Soil under Dicranopteris linearis polluted

PVC:

Soil under P. vittata control

HSD:

Honest significant difference

PCA:

Principal component analysis

ANOVA:

Analysis of variance

CFU:

Colony forming unit

QPCR:

Quantitative real-time polymerase chain reaction

OTU:

Operational taxonomic unit

DGGE:

Denaturing gradient gel electrophoresis

DPPH:

2,2-diphenyl-1-picrylhydrazyl

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Acknowledgments

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.

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Correspondence to Sylvie Nazaret.

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Responsible editor: Philippe Garrigues

Electronic supplementary material

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).

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).

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).

Table S1

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Pham, H.N., Michalet, S., Bodillis, J. et al. Impact of metal stress on the production of secondary metabolites in Pteris vittata L. and associated rhizosphere bacterial communities. Environ Sci Pollut Res 24, 16735–16750 (2017). https://doi.org/10.1007/s11356-017-9167-2

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Keywords

  • Bacterial communities
  • Metal stress
  • Pteris vittata
  • Rhizosphere
  • Secondary metabolites