Extended soil contamination by polychlorinated biphenyls (PCBs) represents a global environmental issue that can hardly be addressed with the conventional remediation treatments. Rhizoremediation is a sustainable alternative, exploiting plants to stimulate in situ the degradative bacterial communities naturally occurring in historically polluted areas. This approach can be enhanced by the use of bacterial strains that combine PCB degradation potential with the ability to promote plant and root development. With this aim, we established a collection of aerobic bacteria isolated from the soil of the highly PCB-polluted site "SIN Brescia-Caffaro" (Italy) biostimulated by the plant Phalaris arundinacea. The strains, selected on biphenyl and plant secondary metabolites provided as unique carbon source, were largely dominated by Actinobacteria and a significant number showed traits of interest for remediation, harbouring genes homologous to bphA, involved in the PCB oxidation pathway, and displaying 2,3-catechol dioxygenase activity and emulsification properties. Several strains also showed the potential to alleviate plant stress through 1-aminocyclopropane-1-carboxylate deaminase activity. In particular, we identified three Rhodococcus strains able to degrade in vitro several PCB congeners and to promote lateral root emergence in the model plant Arabidopsis thaliana in vivo. In addition, these strains showed the capacity to colonize the root system and to increase the plant biomass in PCB contaminated soil, making them ideal candidates to sustain microbial-assisted PCB rhizoremediation through a bioaugmentation approach.

Departement of Biochemistry and Microbiology University of Chemistry and Technology Prague Prague Czech Republic

Department of Food Environmental and Nutritional Sciences University of Milan Milan Italy

Institute of Microbiology Czech Academy of Sciences Prague Czech Republic

Zobrazit více v PubMed

Gioia R, Akindele A J, Adebusoye S A, Asante K A, Tanabe S, Buekens A et al. 2014. Polychlorinated biphenyls (PCBs) in Africa: a review of environmental levels. PubMed DOI

Dvorska A, Lammel G, Klanova J, Holoubek I. 2008. Kosetice, Czech Republic–ten years of air pollution monitoring and four years of evaluating the origin of persistent organic pollutants. PubMed DOI

Hermanson M H, Johnson G W. 2007. Polychlorinated biphenyls in tree bark near a former manufacturing plant in Anniston, Alabama. PubMed DOI

Turrio-Baldassarri L, Abate V, Alivernini S, Battistelli C L, Carasi S, Casella M et al. 2007. A study on PCB, PCDD/PCDF industrial contamination in a mixed urban-agricultural area significantly affecting the food chain and the human exposure. Part I: Soil and feed. PubMed DOI

Xing Y, Lu Y, Dawson R W, Shi Y, Zhang H, Wang T et al. 2005. A spatial temporal assessment of pollution from PCBs in China. PubMed DOI

Beyer A, Biziuk M. 2009. Environmental fate and global distribution of polychlorinated biphenyls. Reviews of Environmental Contamination and Toxicology 201:137–158. 10.1007/978-1-4419-0032-6_5 PubMed DOI

Jepson P D, Deaville R, Barber J L, Aguilar A, Borrell A, Murphy S et al. 2016. PCB pollution continues to impact populations of orcas and other dolphins in European waters. PubMed DOI PMC

Di Guardo A, Terzaghi E, Raspa G, Borin S, Mapelli F, Chouaia B et al. 2017. Differentiating current and past PCB and PCDD/F sources: The role of a large contaminated soil site in an industrialized city area. PubMed DOI

http://www.salute.gov.it/imgs/C_17_pubblicazioni_821_allegato.pdf

Gomes H I, Dias-Ferreira C, Ribeiro A B. 2013. Overview of in situ and ex situ remediation technologies for PCB-contaminated soils and sediments and obstacles for full-scale application. PubMed DOI

Segura A, Rodríguez-Conde S, Ramos C, Ramos J L. 2009. Bacterial responses and interactions with plants during rhizoremediation. PubMed DOI PMC

Terzaghi E, Zanardini E, Morosini C, Raspa G, Borin S, Mapelli F et al. 2018. Rhizoremediation half-lives of PCBs: Role of congener composition, organic carbon forms, bioavailability, microbial activity, plant species and soil conditions, on the prediction of fate and persistence in soil. PubMed DOI

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

Ancona V, Caracciolo A B, Grenni P, Di Lenola M, Campanale C, Calabrese A et al. 2016. Plant-assisted bioremediation of a historically PCB and heavy metal-contaminated area in Southern Italy. PubMed DOI

Vergani L, Mapelli F, Zanardini E, Terzaghi E, Di Guardo A, Morosini C et al. 2017. Phyto-rhizoremediation of polychlorinated biphenyl contaminated soils: An outlook on plant-microbe beneficial interactions. PubMed DOI

Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R et al. 2012. Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149.

Pham T T M, Pino Rodriguez N J, Hijri M, Sylvestre M. 2015. Optimizing polychlorinated biphenyl degradation by flavonoid-induced cells of the rhizobacterium PubMed DOI PMC

LeFevre G H, Hozalsky R M, Novak P J. 2013. Root exudate enhanced contaminant desorption: An abiotic contribution to the rhizosphere effect. PubMed DOI

Musilova L, Ridl J, Polivkova M, Macek T, Uhlik O. 2016. Effects of secondary plant metabolites on microbial populations: changes in community structure and metabolic activity in contaminated environments. PubMed PMC

El Fantroussi S, Agathos S N. 2005. Is bioaugmentation a feasible strategy for pollutant removal and site remediation? PubMed DOI

Thijs S, Van Dillewijn P, Sillen W, Truyens S, Holtappels M, D´Haen J et al. 2014. Exploring the rhizospheric and endophytic bacterialcommunities of

Abhilash P C, Dubey R K, Tripathi V, Gupta V K, Singh H B. 2016. Plant growth-promoting microorganisms for environmental sustainability. PubMed DOI

Terzaghi E, Vergani L, Mapelli F, Borin S, Raspa G, Zanardini E et al. 2019. Rhizoremediation of weathered PCBs in a heavily contaminated agricultural soil: Results of a biostimulation trial in semi field conditions. PubMed DOI

Meggo R E, Schnoor J L. 2013. Rhizospere redox cycling and implications for rhizosphere biotransformation of selected polychlorinated biphenyl (PCB) congeners. PubMed DOI PMC

Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S et al. 2012. A Drought Resistance-Promoting Microbiome Is Selected by Root System under Desert Farming. PubMed DOI PMC

Uhlik O, Strejcek M, Junkova P, Sanda M, Hroudova M, Vlcek C et al. 2011. Matrix-assisted laser desorption ionization (MALDI)–time of flight mass spectrometry- and MALDI biotyper-based identification of cultured biphenyl-metabolizing bacteria from contaminated horseradish rhizosphere soil. Applied and Environmental Microbiology 77:19, 6858–6866. 10.1128/AEM.05465-11 PubMed DOI PMC

Donnelly P K, Hedge R S, Fletcher J S. 1994. Growth of PCB-degrading bacteria on compounds from photosynthetic plants.

Garrido-Sanz D, Manzano J, Martín M, Redondo-Nieto M, Rivilla R. 2008. Metagenomic analysis of a biphenyl-degrading soil bacterial consortium reveals the metabolic roles of specific populations. PubMed DOI PMC

Leigh M B, Prouzova P, Mackova M, Macek T, Nagle D P, Fletcher J S. 2006. Polychlorinated Biphenyl (PCB)-Degrading Bacteria Associated with Trees in a PCB-Contaminated Site. PubMed DOI PMC

Master E R, Mohn W W. 1998. Psychrotolerant Bacteria Isolated from Arctic Soil That Degrade Polychlorinated Biphenyls at Low Temperatures. PubMed PMC

Chouaia B, Rossi P, Montagna M, Ricci I, Crotti E, Damiani C et al. 2010. Molecular evidence for multiple infections as revealed by typing of PubMed DOI PMC

Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A et al. 2013. Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. PubMed DOI PMC

Yoon S H, Ha S M, Kwon S, Lim J, Kim Y, Seo H et al. 2017. Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. PubMed DOI PMC

Leewis M-C, Uhlik O, Leigh M B. 2016. Synergistic processing of biphenyl and benzoate: carbon flow through the bacterial community in polychlorinated-biphenyl- contaminated soil. PubMed DOI PMC

Iwai S, Chai B, Sul W J, Cole J R, Hashsham S A, Tiedje J M. 2010. Gene-targeted-metagenomics reveals extensive diversity of aromatic dioxygenase genes in the environment. PubMed DOI PMC

Margesin R, Gander S, Zacke G, Gounot A M, Schinner F. 2003. Hydrocarbon degradation and enzyme activities of cold-adapted bacteria and yeasts. PubMed DOI

Barbato M, Mapelli F, Magagnini M, Chouaia B, Armeni M, Marasco R et al. 2016. Hydrocarbon pollutants shape bacterial community assembly of harbor sediments. PubMed DOI

Belimov A A, Hontzeas N, Safronova V I, Demchinskaya S V, Piluzza G, Bullitta S et al. 2005. Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard ( DOI

Taniyasu S, Kannan K, Holoubek I, Ansorgova A, Horii Y, Hanari N et al. 2003. Isomer-specific analysis of chlorinated biphenyls, naphthalenes and dibenzofurans in Delor: polychlorinated biphenyl preparations from the former Czechoslovakia. PubMed

Ridl J, Suman J, Fraraccio S, Hradilova M, Strejcek M, Cajthaml T et al. 2018. Complete genome sequence of PubMed DOI PMC

Čvančarová M, Křesinová Z, Filipová A, Covino S, Cajthaml T. 2012. Biodegradation of PCBs by ligninolytic fungi and characterization of the degradation products. PubMed DOI

Masai E, Yamada A, Healy J M, Hatta T, Kimbara K, Fukuda M et al. 1995. Characterization of biphenyl catabolic genes of gram-positive polychlorinated biphenyl degrader PubMed PMC

Vergani L, Mapelli F, Marasco R, Crotti E, Fusi M, Di Guardo A et al. 2017. Bacteria associated to plants naturally selected in a historical PCB polluted soil show potential to sustain natural attenuation. PubMed DOI PMC

Arenskötter M, Bröker D, Steinbüchel A. 2004. Biology of the metabolically diverse genus PubMed DOI PMC

Fu H, Wei Y, Zou Y, Li M, Wang F, Chen J et al. 2014. Research progress on the DOI

Furukawa K, Fujihara H. 2008. Microbial degradation of polychlorinated byphenils: Biochemical and molecular features. PubMed

Fuchs G, Boll M, Heider J. 2011. Microbial degradation of aromatic compounds—from one strategy to four. PubMed DOI

Kügler J K, LeRoes-Hill M, Syldatk C, Hausmann R. 2015. Surfactants tailored by the class PubMed DOI PMC

Passatore L, Rossetti C, Juwarkard A A, Massacci A. 2014. Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): State of knowledge and research perspectives. PubMed DOI

Xu L, Teng Y, Li Z-G, Norton J M, Luo Y-M. 2010. Enhanced removal of polychlorinated biphenyls from alfalfa rhizosphere soil in a field study: The impact of a rhizobial inoculum. PubMed DOI

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

Differential effect of monoterpenes and flavonoids on the transcription of aromatic ring-hydroxylating dioxygenase genes in Rhodococcus opacus C1 and Rhodococcus sp. WAY2

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

Predominant Biphenyl Dioxygenase From Legacy Polychlorinated Biphenyl (PCB)-Contaminated Soil Is a Part of Unusual Gene Cluster and Transforms Flavone and Flavanone

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