Skip to main content

Environmental pollution effects on plant microbiota: the case study of poplar bacterial-fungal response to silver nanoparticles

Applied Microbiology and Biotechnology volume 103, pages 8215–8227 (2019)Cite this article

Abstract

Pollution affects most of the urban and forest environments at different levels causing well-known effects on human and plant health. The influence that pollutants exert on plant-associated microbiota might direct plant health and, in some cases, also the removal of pollutants by plants. With the advent of nanotechnologies, an increasing amount of engineered nanoparticles are being introduced into the environment, and consequently, their impact on plant-associated microorganisms needs to be investigated. In this context, silver nanoparticles (Ag-NPs) were experimentally supplied at leaf and root level of poplar plants to assess Ag-NPs effects on plant microbiota. Leaf Ag-NP treatment increased bacteria and fungi evenness and determined a significant reduction in both microbial groups, while root Ag-NP treatment reduced the bacterial and fungal biodiversity. Bioinformatics functional analysis showed that Ag-NP treatment reduced the aerobic and stimulated facultative anaerobic and oxidative stress-tolerant bacteria. Our study offers new insights into the effects of Ag-NPs on both phyllosphere and rhizosphere poplar-associated microbiota and may represent a first attempt to understand the behavior of microbial communities of a tree species growing in a polluted environment.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

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

References

  • Akbar A, Anal AK (2014) Zinc oxide nanoparticles loaded active packaging, a challenge study against Salmonella typhimurium and Staphylococcus aureus in ready-to-eat poultry meat. Food Control 38:88–95

    Article  CAS  Google Scholar 

  • Albanese D, Fontana P, De Filippo C, Cavalieri D, Donati C (2015) MICCA: a complete and accurate software for taxonomic profiling of metagenomic data. Sci Rep 5:9743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Ali S, Charles TC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167

    Article  CAS  PubMed  Google Scholar 

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. In: Babraham bioinformatics. http://www.bioinformatics.babraham.ac.uk/projects/fastqc

  • Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M, Dombrowski N, Münch PC, Spaepen S, Remus-Emsermann M, Hüttel B, McHardy AC, Vorholt JA, Schulze-Lefert P (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–369

    Article  CAS  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  PubMed  Google Scholar 

  • Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    Article  CAS  PubMed  Google Scholar 

  • Bravin MN, Garnier C, Lenoble V, Gérard F, Dudal Y, Hinsinger P (2012) Root-induced changes in pH and dissolved organic matter binding capacity affect copper dynamic speciation in the rhizosphere. Geochim Cosmochim Acta 84:256–268

    Article  CAS  Google Scholar 

  • Bystrzejewska-Piotrowska G, Golimowski J, Urban PL (2009) Nanoparticles: their potential toxicity, waste and environmental management. Waste Manag 29:2587–2595

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, Belausov E, Hunter MS, Zchori-Fein E (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc Biol Sci 279:1791–1796

    Article  CAS  PubMed  Google Scholar 

  • Ceballos I, Ruiz M, Fernandez C, Pena R, Rodriguez A, Sanders IR (2013) The in vitro mass-produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS One 8:e70633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cocozza C, Vitullo D, Lima G, Maiuro L, Marchetti M, Tognetti R (2014) Enhancing phytoextraction of cd by combining poplar (clone “I-214”) with Pseudomonas fluorescens and microbial consortia. Environ Sci Pollut Res Int 21:1796–1808

    Article  CAS  PubMed  Google Scholar 

  • Cocozza C, Trupiano D, Lustrato G, Alfano G, Vitullo D, Falasca A, Lomaglio T, De Felice V, Lima G, Ranalli G, Scippa S, Tognetti R (2015) Challenging synergistic activity of poplar–bacteria association for the cd phytostabilization. Environ Sci Pollut Res 22:19546–19561

    Article  CAS  Google Scholar 

  • Cocozza C, Perone A, Giordano C, Salvatici MC, Pignattelli S, Raio A, Schaub M, Sever K, Innes JL, Tognetti R, Cherubini P (2019) Silver nanoparticles enter the tree stem faster through leaves than through roots. Tree Physiol 39:1251–1261. https://doi.org/10.1093/treephys/tpz046

    Article  CAS  PubMed  Google Scholar 

  • de Lima R, Seabra AB, Durán N (2012) Silver nanoparticles: a brief review of cytotoxicity and genotoxicity of chemically and biogenically synthesized nanoparticles. J Appl Toxicol 32:867–879

    Article  CAS  PubMed  Google Scholar 

  • Dietz KJ, Herth S (2011) Plant nanotoxicology. Trends Plant Sci 16:582–589

    Article  CAS  PubMed  Google Scholar 

  • Dimkpa CO, McLean JE, Martineau N, Britt DW, Haverkamp R, Anderson AJ (2013) Silver nanoparticles disrupt wheat (Triticum aestivum L.) growth in a sand matrix. Environ Sci Technol 47:1082–1109

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv 081257

  • Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43:7285–7290

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Cui X, He S, Dong G, Chen M, Wang J, Lin X (2013) The role of metal nanoparticles in influencing arbuscular mycorrhizal fungi effects on plant growth. Environ Sci Technol 47:9496–9504

    Article  CAS  PubMed  Google Scholar 

  • Fernandez CW, Kennedy PG (2018) Melanization of mycorrhizal fungal necromass structures microbial decomposer communities. J Ecol 106:468–479

    Article  CAS  Google Scholar 

  • Ferrari B, Winsley T, Ji M, Neilan B (2014) Insights into the distribution and abundance of the ubiquitous candidatus Saccharibacteria phylum following tag pyrosequencing. Sci Rep 4:3957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M, Karpinets T, Uberbacher E, Tuskan GA, Vilgalys R, Doktycz MJ, Schadt CW (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77:5934–5944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gramaje D, Úrbez-Torres JR, Sosnowski MR (2018) Managing grapevine trunk diseases with respect to etiology and epidemiology: current strategies and future prospects. Plant Dis 102:12–39

    Article  PubMed  Google Scholar 

  • Haichar F e Z, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  CAS  PubMed  Google Scholar 

  • Jain P, Pundir RK (2017) Potential role of endophytes in sustainable agriculture-recent developments and future prospects. In: Maheshwari DK (ed) Endophytes: biology and biotechnology: volume 1. Springer International Publishing, Cham, pp 145–169

    Chapter  Google Scholar 

  • Joshi NA, Fass JN (2011) Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files (version 1.33)[software]

  • Kandlikar GS, Gold ZJ, Cowen MC, Meyer RS, Freise AC, Kraft N, Moberg-Parker J, Sprague J, Kushner DJ, Curd EE (2018) Ranacapa: an R package and shiny web app to explore environmental DNA data with exploratory statistics and interactive visualizations. F1000Research 7:1734

    Article  PubMed  PubMed Central  Google Scholar 

  • Kawasaki S, Moriguchi R, Sekiya K, Nakai T, Ono E, Kume K, Kawahara K (1994) The cell envelope structure of the lipopolysaccharide-lacking gram-negative bacterium Sphingomonas paucimobilis. J Bacteriol 176:284–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kembel SW, Mueller RC (2014) Plant traits and taxonomy drive host associations in tropical phyllosphere fungal communities. Botany 92:303–311

    Article  Google Scholar 

  • Klasen HJ (2000) A historical review of the use of silver in the treatment of burns. II Renewed interest for silver. Burns 26:131–138

    Article  CAS  PubMed  Google Scholar 

  • Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucl Ac Res 41(1):e1

    Article  CAS  Google Scholar 

  • Koizumi Y, Yamada R, Nishioka M, Matsumura Y, Tsuchido T, Taya M (2002) Deactivation kinetics of Escherichia coli cells correlated with intracellular superoxide dismutase activity in photoreaction with titanium dioxide particles. J Chem Technol Biotechnol 77:671–677

    Article  CAS  Google Scholar 

  • Kolton M, Erlacher A, Berg G, Cytryn E (2016) The Flavobacterium genus in the plant holobiont: ecological, physiological, and applicative insights. In: Microbial models: from environmental to industrial sustainability. Springer, Singapore, pp 189–207

    Chapter  Google Scholar 

  • Lahti L, Sudarshan S (2017) Microbiome R package. http://microbiome.github.com/microbiome

  • Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Y, He X, Zhang P, Zhang Z, Guo Z, Tai R, Xu Z, Zhang L, Ding Y, Zhao Y, Chai Z (2011) Phytotoxicity and biotransformation of La2O3 nanoparticles in a terrestrial plant cucumber (Cucumis sativus). Nanotoxicology 5:743–753

    Article  CAS  PubMed  Google Scholar 

  • Maillard JY, Hartemann P (2012) Silver as an antimicrobial: facts and gaps in knowledge. Crit Rev Microbiol 39:373–383

    Article  CAS  PubMed  Google Scholar 

  • Majeed A, Muhammad Z, Ahmad H (2018) Plant growth promoting bacteria: role in soil improvement, abiotic and biotic stress management of crops. Plant Cell Rep 37:1599–1609

    Article  CAS  PubMed  Google Scholar 

  • Mapperson RR, Kotiw M, Davis RA, Dearnaley JDW (2014) The diversity and antimicrobial activity of Preussia sp. endophytes isolated from Australian dry rainforests. Curr Microbiol 68:30–37

    Article  CAS  PubMed  Google Scholar 

  • Marques JM, da Silva TF, Vollu RE, Blank AF, Ding G-C, Seldin L, Smalla K (2014) Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. FEMS Microbiol Ecol 88:424–435

    Article  CAS  PubMed  Google Scholar 

  • McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618

    Article  CAS  PubMed  Google Scholar 

  • McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663

    Article  CAS  PubMed  Google Scholar 

  • Menkis A, Marčiulynas A, Gedminas A, Lynikienė J, Povilaitienė A (2015) High-throughput sequencing reveals drastic changes in fungal communities in the phyllosphere of Norway spruce (Picea abies) following invasion of the spruce bud scale (Physokermes piceae). Microb Ecol 70:904–911

    Article  CAS  PubMed  Google Scholar 

  • Nan X (2018) ggsci: scientific journal and sci-fi themed color palettes for “ggplot2.” https://CRAN.R-project.org/package=ggsci

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Article  Google Scholar 

  • Nowack B, Ranville JF, Diamond S, Gallego-Urrea JA, Metcalfe C, Rose J, Horne N, Koelmans AA, Klaine SJ (2012) Potential scenarios for nanomaterial release and subsequent alteration in the environment. Environ Toxicol Chem 31:50–59

    Article  CAS  PubMed  Google Scholar 

  • Pallavi MCM, Srivastava R, Arora S, Sharma AK (2016) Impact assessment of silver nanoparticles on plant growth and soil bacterial diversity. 3 Biotech 6:254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  CAS  PubMed  Google Scholar 

  • Paulson JN, Stine OC, Bravo HC, Pop M (2013) Differential abundance analysis for microbial marker-gene surveys. Nat Methods 10(12):1200–1202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prodi A, Sandalo S, Tonti S, Nipoti P, Pisi A (2008) Phialophora-like fungi associated with kiwifruit elephantiasis. J Plant Pathol 90:487–494

    CAS  Google Scholar 

  • Pulit-Prociack J, Banach M (2016) Silver nanoparticles - a material of the future…? Open Chem 14:76–91

    Google Scholar 

  • Qiao Q, Wang F, Zhang J, Chen Y, Zhang C, Liu G, Zhang H, Ma C, Zhang J (2017) The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Sci Rep 7:3940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. https://www.R-project.org/. 2018

  • Rai M, Rathod D, Agarkar G, Dar M, Brestic M, Pastore GM, Junior MRM (2014) Fungal growth promotor endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79

    Article  CAS  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574

    Article  CAS  PubMed  Google Scholar 

  • Regier N, Streb S, Cocozza C, Schaub M, Cherubini P, Zeeman SC, Frey B (2009) Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. Plant Cell Environ 32:1724–1736

    Article  CAS  PubMed  Google Scholar 

  • Shahrokh S, Hosseinkhani B, Emtiazi G (2014) The impact of silver nanoparticles on bacterial aerobic nitrate reduction process. J Bioprocess Biotech 4:152

    Article  CAS  Google Scholar 

  • Sillen WMA, Thijs S, Abbamondi GR, Janssen J, Weyens N, White JC, Vangronsveld J (2015) Effects of silver nanoparticles on soil microorganisms and maize biomass are linked in the rhizosphere. Soil Biol Biochem 91:14–22

    Article  CAS  Google Scholar 

  • Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341–353

    Article  CAS  PubMed  Google Scholar 

  • Simonin M, Richaume A (2015) Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review. Environ Sci Pollut Res 22:13710–13723

    Article  CAS  Google Scholar 

  • Suyal DC, Shukla A, Goel R (2014) Growth promotory potential of the cold adapted diazotroph Pseudomonas migulae S10724 against native green gram (Vigna radiata (L.) Wilczek). 3 Biotech 4:665–668

    Article  PubMed  PubMed Central  Google Scholar 

  • Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417

    Article  CAS  PubMed  Google Scholar 

  • Travadon R, Lawrence DP, Rooney-Latham S, Gubler WD, Wilcox WF, Rolshausen PE, Baumgartner K (2015) Cadophora species associated with wood-decay of grapevine in North America. Fungal Biol 119:53–66

    Article  PubMed  Google Scholar 

  • Tripathi DK, Tripathi A, Shweta SS, Singh Y, Vishwakarma K, Yadav G, Sharma S, Singh VK, Mishra RK, Upadhyay RG, Dubey NK, Lee Y, Chauhan DK (2017) Uptake, accumulation and toxicity of silver nanoparticle in autotrophic plants, and heterotrophic microbes: a concentric review. Front Microbiol 8:07

    PubMed  PubMed Central  Google Scholar 

  • Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaz-Moreira I, Nunes OC, Manaia CM (2011) Diversity and antibiotic resistance patterns of Sphingomonadaceae isolates from drinking water. Appl Environ Microbiol 77:5697–5706

  • Vittori Antisari L, Lo Papa G, Ferronato C, Falsone G, Vianello G, Dazzi C (2014) In situ remediation of polluted Spolic Technosols using Ca(OH)2 and smectitic marlstone. Geoderma 232-234:1–9

  • Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Chang L-Y, Wang Y-J, Wang Q, Yang C-H, Mei R-H (2009) Nanoparticles affect the survival of bacteria on leaf surfaces. FEMS Microbiol Ecol 68:182–191

    Article  CAS  PubMed  Google Scholar 

  • Wang W-N, Tarafdar JC, Biswas P (2013) Nanoparticle synthesis and delivery by an aerosol route for watermelon plant foliar uptake. J Nanopart Res 15. https://doi.org/10.1007/s11051-013-1417-8

  • Wang P, Lombi E, Zhao F-J, Kopittke PM (2016) Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci 21:699–712

    Article  CAS  PubMed  Google Scholar 

  • Ward T, Larson J, Meulemans J, Hillmann B, Lynch J, Sidiropoulos D, Spear J, Caporaso G, Blekhman R, Knight R, Fink R, Knights D (2017) BugBase predicts organism level microbiome phenotypes. bioRxiv. https://doi.org/10.1101/133462

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Wilkinson L (2011) ggplot2: elegant graphics for data analysis by Wickham, H. Biometrics 67:678–679

    Article  Google Scholar 

  • Yin L, Colman BP, McGill BM, Wright JP, Bernhardt ES (2012) Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS One 7:e47674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina paired-end read merger. Bioinformatics 30:614–620

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Authors thank Annalisa Perone and Sara Pignattelli for the contribution in the lab activities.

Author information

Author notes

  1. Francesco Vitali and Aida Raio contributed equally to this work.

Authors and Affiliations

  1. Dipartimento di Biologia, Università degli Studi di Firenze, 50019, Sesto Fiorentino, Italy

    Francesco Vitali & Duccio Cavalieri

  2. Istituto di Biometeorologia, IBIMET-CNR, 50019, Sesto Fiorentino, Italy

    Francesco Vitali

  3. Istituto per la Protezione Sostenibile delle Piante, IPSP-CNR, 50019, Sesto Fiorentino, Italy

    Aida Raio & Federico Sebastiani

  4. Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zürcherstrasse 111, 8903, Birmensdorf, Switzerland

    Paolo Cherubini

  5. Department of Agriculture, Food, Environment and Forestry, University of Florence, 50145, Florence, Italy

    Claudia Cocozza

Authors
  1. Francesco Vitali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aida Raio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Federico Sebastiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paolo Cherubini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Duccio Cavalieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Claudia Cocozza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Federico Sebastiani.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(PDF 480 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vitali, F., Raio, A., Sebastiani, F. et al. Environmental pollution effects on plant microbiota: the case study of poplar bacterial-fungal response to silver nanoparticles. Appl Microbiol Biotechnol 103, 8215–8227 (2019). https://doi.org/10.1007/s00253-019-10071-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-019-10071-2

Keywords

  • Poplar
  • Silver-nanoparticles
  • Phyllosphere microbiota
  • Rhizosphere microbiota
  • 16S rRNA metabarcoding
  • ITS metabarcoding