Despite decades of research there is limited understanding of how vegetation impacts the ability of microbial communities to process organic contaminants in soil. Using a combination of traditional and molecular assays, we examined how phytoremediation with willow and/or fertilization affected the microbial community present and active in the transformation of diesel contaminants. In a pot study, willow had a significant role in structuring the total bacterial community and resulted in significant decreases in diesel range organics (DRO). However, stable isotope probing (SIP) indicated that fertilizer drove the differences seen in community structure and function. Finally, analysis of the total variance in both pot and SIP experiments indicated an interactive effect between willow and fertilizer on the bacterial communities. This study clearly demonstrates that a willow native to Alaska accelerates DRO degradation, and together with fertilizer, increases aromatic degradation by shifting microbial community structure and the identity of active naphthalene degraders.

Department of Biochemistry and Microbiology Faculty of Food and Biochemical Technology University of Chemistry and Technology Prague Czech Republic

Institute of Arctic Biology University of Alaska Fairbanks Fairbanks AK USA

Zobrazit více v PubMed

Abbasian F., Lockington R., Megharaj M., Naidu R. (2015). A review on the genetics of aliphatic and aromatic hydrocarbon degradation. PubMed DOI

Agency for Toxic Substances and Disease Registry (1999). PubMed

Agrawal A. A., Fishbein M. (2006). Plant defense syndromes. PubMed DOI

Anderson M. J. (2001). A new method for non-parametric multivariate analysis of variance. DOI

Argus G. W. (1999). Classification of salix in the new world.

Badri D. V., Weir T. L., Van Der Lelie D., Vivanco J. M. (2009). Rhizosphere chemical dialogues: plant–microbe interactions. PubMed DOI

Benizri E., Amiaud B. (2005). Relationship between plants and soil microbial communities in fertilized grasslands. DOI

Berry D., Ben Mahfoudh K., Wagner M., Loy A. (2011). Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. PubMed DOI PMC

Bossert I., Bartha R. (1984). “The fate of petroleum in soil ecosystems,” in

Bryant J. P., Reichardt P. B., Clausen T. P. (1992). Chemically mediated interactions between woody plants and browsing mammals. DOI

Bushnell L. D., Haas H. F. (1941). The utilization of certain hydrocarbons by microorganisms. PubMed PMC

Chen S.-H., Aitken M. D. (1999). Salicylate stimulates the degradation of high-molecular weight polycyclic aromatic hydrocarbons by DOI

Dakora F. D., Phillips D. A. (2002). Root exudates as mediators of mineral acquisition in low-nutrient environments. DOI

de Man J. C. (1983). MPN tables, corrected. DOI

Dennis P. G., Miller A. J., Hirsch P. R. (2010). Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? PubMed DOI

Dunn N. W., Gunsalus I. C. (1973). Transmissible plasmid coding early enzymes of naphthalene oxidation in PubMed PMC

Fields M. J., Orians C. M. (2006). Specificity of phenolic glycoside induction in willow seedlings ( PubMed DOI

Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., et al. (1993). Requirement of salicylic acid for the induction of systemic acquired resistance. PubMed DOI

Haines J. R., Wrenn B. A., Holder E. L., Strohmeier K. L., Herrington R. T., Venosa A. D. (1996). Measurement of hydrocarbon-degrading microbial populations by a 96-well plate most-probable-number procedure. PubMed DOI

Harayama S., Timmis K. N. (1989). “Catabolism of aromatic hydrocarbons by

Hartmann A., Schmid M., Van Tuinen D., Berg G. (2009). Plant-driven selection of microbes. DOI

Johnson D., Kershaw L. J., Mackinnon A., Pojar J. (2009).

Jones M. D., Crandell D. W., Singleton D. R., Aitken M. D. (2011). Stable-isotope probing of the polycyclic aromatic hydrocarbon-degrading bacterial guild in a contaminated soil. PubMed DOI PMC

Juhasz A. L., Naidu R. (2000). Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. DOI

Julkunen-Tiitto R. (1985). Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. DOI

Julkunentiitto R. (1989). Phenolic constituents of DOI

Khan S., Afzal M., Iqbal S., Khan Q. M. (2013). Plant–bacteria partnerships for the remediation of hydrocarbon contaminated soils. PubMed DOI

Kuiper I., Lagendijk E. L., Bloemberg G. V., Lugtenberg B. J. (2004). Rhizoremediation: a beneficial plant-microbe interaction. PubMed DOI

Kurzawová V., Štursa P., Uhlík O., Norková K., Strohalm M., Lipov J., et al. (2012). Plant-microorganism interactions in bioremediation of polychlorinated biphenyl-contaminated soil. PubMed DOI

Leewis M. C., Reynolds C. M., Leigh M. B. (2013). Long-term effects of nutrient addition and phytoremediation on diesel and crude oil contaminated soils in subarctic Alaska. PubMed DOI PMC

Leff J. W., Jones S. E., Prober S. M., Barberán A., Borer E. T., Firn J. L., et al. (2015). Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. PubMed DOI PMC

Leigh M. B., Fletcher J. S., Fu X., Schmitz F. J. (2002). Root turnover: an important source of microbial substrates in rhizosphere remediation of recalcitrant contaminants. PubMed DOI

Liliensiek A.-K., Thakuria D., Clipson N. (2012). Influences of plant species composition, fertilisation and lolium perenne ingression on soil microbial community structure in three irish grasslands. PubMed DOI

Lu X.-Y., Zhang T., Fang H.-P. (2011). Bacteria-mediated PAH degradation in soil and sediment. PubMed DOI

Macek T., Macková M., Káš J. (2000). Exploitation of plants for the removal of organics in environmental remediation. PubMed DOI

Macková M., Dowling D., Macek T. (eds) (2006).

Neumann G., George T. S., Plassard C. (2009). Strategies and methods for studying the rhizosphere—the plant science toolbox. DOI

Nováková M., Šašek V., Dobrev P. I., Valentová O., Burketová L. (2014). Plant hormones in defense response of Brassica napus to Sclerotinia sclerotiorum – reassessing the role of salicylic acid in the interaction with a necrotroph. PubMed DOI

Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O’hara R. B., et al. (2013).

Pagé A. P., Yergeau É., Greer C. W. (2015). Salix purpurea stimulates the expression of specific bacterial xenobiotic degradation genes in a soil contaminated with hydrocarbons. PubMed DOI PMC

Pulford I. D., Watson C. (2003). Phytoremediation of heavy metal-contaminated land by trees—a review. PubMed DOI

R Development Core Team (2009).

Rock S. A., Sayre P. G. (1998). Phytoremediation of hazardous wastes: potential regulatory acceptability. DOI

Rosselló-Mora R. A., Lalucat J., García-Valdés E. (1994). Comparative biochemical and genetic analysis of naphthalene degradation among PubMed PMC

Salt D. E., Smith R. D., Raskin I. (1998). Phytoremediation. PubMed DOI

Schell M. A. (1985). Transcriptional control of the nah and sal hydrocarbon-degradation operons by the nahR gene product. PubMed DOI

Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. PubMed DOI PMC

Schnoor J. L., Licht L. A., Mccutcheon S. C., Wolfe N. L., Carreira L. H. (1995). Phytoremediation of organic and nutrient contaminants. PubMed DOI

Schwab A. P., Su J., Wetzel S., Pekarek S., Banks M. K. (1999). Extraction of petroleum hydrocarbons from soil by mechanical shaking. DOI

Siciliano S. D., Germida J. J. (1998). Mechanisms of phytoremediation: biochemical and ecological interactions between plants and bacteria. DOI

Siciliano S. D., Germida J. J., Banks K., Greer C. W. (2003). Changes in microbial community composition and function during a polyaromatic hydrocarbon phytoremediation field trial. PubMed DOI PMC

Singer A. C., Crowley D. E., Thompson I. P. (2003). Secondary plant metabolites in phytoremediation and biotransformation. PubMed DOI

Singleton D. R., Guzmán Ramirez L., Aitken M. D. (2009). Characterization of a polycyclic aromatic hydrocarbon degradation gene cluster in a phenanthrene-degrading acidovorax strain. PubMed DOI PMC

Slater H., Gouin T., Leigh M. B. (2011). Assessing the potential for rhizoremediation of PCB contaminated soils in northern regions using native tree species. PubMed DOI PMC

Su J.-Q., Ding L.-J., Xue K., Yao H.-Y., Quensen J., Bai S.-J., et al. (2015). Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. PubMed DOI

Tanaka M., Nakamura M. (2015). Spatially distinct responses within willow to bark stripping by deer: effects on insect herbivory. PubMed DOI

Toussaint J.-P., Pham T., Barriault D., Sylvestre M. (2012). Plant exudates promote PCB degradation by a rhodococcal rhizobacteria. PubMed DOI

Trapp S., Köhler A., Larsen L. C., Zambrano K. C., Karlson U. (2001). Phytotoxicity of fresh and weathered diesel and gasoline to willow and poplar trees. DOI

Uhlík O., Ječná K., Macková M., Vlček C., Hroudová M., Demnerová K., et al. (2009). Biphenyl-metabolizing bacteria in the rhizosphere of horseradish and bulk soil contaminated by polychlorinated biphenyls as revealed by stable isotope probing. PubMed DOI PMC

Uhlík O., Wald J., Strejček M., Musilová L., Rídl J., Hroudová M., et al. (2012). Identification of bacteria utilizing biphenyl, benzoate, and naphthalene in long-term contaminated soil. PubMed DOI PMC

Wald J., Hroudová M., Jansa J., Vrchotová B., Macek T., Uhlík O. (2015). Pseudomonads rule degradation of polyaromatic hydrocarbons in aerated sediment. PubMed DOI PMC

White J. R., Nagarajan N., Pop M. (2009). Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PubMed DOI PMC

Whiteley A. S., Wiles S., Lilley A. K., Philp J., Bailey M. J. (2001). Ecological and physiological analyses of PubMed DOI

Yergeau E., Sanschagrin S., Maynard C., St-Arnaud M., Greer C. W. (2014). Microbial expression profiles in the rhizosphere of willows depend on soil contamination. PubMed DOI PMC

Yi H., Crowley D. E. (2007). Biostimulation of PAH degradation with plants containing high concentrations of linoleic acid. PubMed DOI

Legacy Effects of Phytoremediation on Plant-Associated Prokaryotic Communities in Remediated Subarctic Soil Historically Contaminated with Petroleum Hydrocarbons

DNA stable isotope probing on soil treated by plant biostimulation and flooding revealed the bacterial communities involved in PCB degradation

Biphenyl 2,3-Dioxygenase in Pseudomonas alcaliphila JAB1 Is Both Induced by Phenolics and Monoterpenes and Involved in Their Transformation

Genomic analysis of dibenzofuran-degrading Pseudomonas veronii strain Pvy reveals its biodegradative versatility

Effects of Secondary Plant Metabolites on Microbial Populations: Changes in Community Structure and Metabolic Activity in Contaminated Environments

Plants Rather than Mineral Fertilization Shape Microbial Community Structure and Functional Potential in Legacy Contaminated Soil