Cis-1,2-dichloroethylene (cDCE), which is a common hazardous compound, often accumulates during incomplete reductive dechlorination of higher chlorinated ethenes (CEs) at contaminated sites. Simple monoaromatics, such as toluene and phenol, have been proven to induce biotransformation of cDCE in microbial communities incapable of cDCE degradation in the absence of other carbon sources. The goal of this microcosm-based laboratory study was to discover non-toxic natural monoaromatic secondary plant metabolites (SPMEs) that could enhance cDCE degradation in a similar manner to toluene and phenol. Eight SPMEs were selected on the basis of their monoaromatic molecular structure and widespread occurrence in nature. The suitability of the SPMEs chosen to support bacterial growth and to promote cDCE degradation was evaluated in aerobic microbial cultures enriched from cDCE-contaminated soil in the presence of each SPME tested and cDCE. Significant cDCE depletions were achieved in cultures enriched on acetophenone, phenethyl alcohol, p-hydroxybenzoic acid and trans-cinnamic acid. 16S rRNA gene sequence analysis of each microbial community revealed ubiquitous enrichment of bacteria affiliated with the genera Cupriavidus, Rhodococcus, Burkholderia, Acinetobacter and Pseudomonas. Our results provide further confirmation of the previously stated secondary compound hypothesis that plant metabolites released into the rhizosphere can trigger biodegradation of environmental pollutants, including cDCE.

Technical University of Liberec Liberec Czech Republic

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

Zobrazit více v PubMed

Olaniran AO, Pillay D, Pillay B. Chloroethenes contaminants in the environment: Still a cause for concern. Afr. J. Biotechnol. 2004;3:675–682.

Agency for Toxic Substances and Disease Registry. Toxicological Profile for 1,2-Dichloroethene, https://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=464&tid=82 (1996). PubMed

Tiehm A, Schmidt KR. Sequential anaerobic/aerobic biodegradation of chloroethenes–aspects of field application. Curr. Opin. Biotechnol. 2011;22:415–421. doi: 10.1016/j.copbio.2011.02.003. PubMed DOI

Smidt H, de Vos WM. Anaerobic microbial dehalogenation. Annu. Rev. Microbiol. 2004;58:43–73. doi: 10.1146/annurev.micro.58.030603.123600. PubMed DOI

Field JA, Sierra-Alvarez R. Biodegradability of chlorinated solvents and related chlorinated aliphatic compounds. Rev. Environ. Sci. Biotechnol. 2004;3:185–254. doi: 10.1007/s11157-004-4733-8. DOI

Bhatt P, Kumar MS, Mudliar S, Chakrabarti T. Biodegradation of chlorinated compounds—a review. Crit. Rev. Environ. Sci. Technol. 2007;37:165–198. doi: 10.1080/10643380600776130. DOI

Maymo-Gatell X, Chien Y-t, Gossett JM, Zinder SH. Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science. 1997;276:1568–1571. doi: 10.1126/science.276.5318.1568. PubMed DOI

Cupples AM, Spormann AM, McCarty PL. Growth of a Dehalococcoides-like microorganism on vinyl chloride and cis-dichloroethene as electron acceptors as determined by competitive PCR. Appl. Environ. Microbiol. 2003;69:953–959. doi: 10.1128/AEM.69.2.953-959.2003. PubMed DOI PMC

Löffler FE, et al. Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum. Chloroflexi. Int. J. Syst. Evol. Microbiol. 2013;63:625–635. doi: 10.1099/ijs.0.034926-0. PubMed DOI

Schmidt K, Tiehm A. Natural attenuation of chloroethenes: identification of sequential reductive/oxidative biodegradation by microcosm studies. Water Sci. Technol. 2008;58:1137–1145. doi: 10.2166/wst.2008.729. PubMed DOI

Kielhorn J, Melber C, Wahnschaffe U, Aitio A, Mangelsdorf I. Vinyl chloride: still a cause for concern. Environ. Health Perspect. 2000;108:579. doi: 10.1289/ehp.00108579. PubMed DOI PMC

Mattes TE, Alexander AK, Coleman NV. Aerobic biodegradation of the chloroethenes: pathways, enzymes, ecology, and evolution. FEMS Microbiol. Rev. 2010;34:445–475. doi: 10.1111/j.1574-6976.2010.00210.x. PubMed DOI

Coleman NV, Mattes TE, Gossett JM, Spain JC. Biodegradation of cis-dichloroethene as the sole carbon source by a β-proteobacterium. Appl. Environ. Microbiol. 2002;68:2726–2730. doi: 10.1128/AEM.68.6.2726-2730.2002. PubMed DOI PMC

Mattes TE, et al. The genome of Polaromonas sp. strain JS666: insights into the evolution of a hydrocarbon-and xenobiotic-degrading bacterium, and features of relevance to biotechnology. Appl. Environ. Microbiol. 2008;74:6405–6416. doi: 10.1128/AEM.00197-08. PubMed DOI PMC

Jennings LK, et al. Proteomic and transcriptomic analyses reveal genes upregulated by cis-dichloroethene in Polaromonas sp. strain JS666. Appl. Environ. Microbiol. 2009;75:3733–3744. doi: 10.1128/AEM.00031-09. PubMed DOI PMC

Olaniran AO, Pillay D, Pillay B. Aerobic biodegradation of dichloroethenes by indigenous bacteria isolated from contaminated sites in Africa. Chemosphere. 2008;73:24–29. doi: 10.1016/j.chemosphere.2008.06.003. PubMed DOI

Bradley PM, Chapelle FH. Aerobic microbial mineralization of dichloroethene as sole carbon substrate. Environ. Sci. Technol. 2000;34:221–223. doi: 10.1021/es990785c. DOI

Schmidt KR, Augenstein T, Heidinger M, Ertl S, Tiehm A. Aerobic biodegradation of cis-1,2-dichloroethene as sole carbon source: Stable carbon isotope fractionation and growth characteristics. Chemosphere. 2010;78:527–532. doi: 10.1016/j.chemosphere.2009.11.033. PubMed DOI

Rojo F. Specificity at the end of the tunnel: understanding substrate length discrimination by the AlkB alkane hydroxylase. J. Bacteriol. 2005;187:19–22. doi: 10.1128/JB.187.1.19-22.2005. PubMed DOI PMC

Behrendorff JB, Huang W, Gillam EM. Directed evolution of cytochrome P450 enzymes for biocatalysis: exploiting the catalytic versatility of enzymes with relaxed substrate specificity. Biochem. J. 2015;467:1–15. doi: 10.1042/BJ20141493. PubMed DOI

Arp DJ, Yeager CM, Hyman MR. Molecular and cellular fundamentals of aerobic cometabolism of trichloroethylene. Biodegradation. 2001;12:81–103. doi: 10.1023/A:1012089908518. PubMed DOI

Le NB, Coleman NV. Biodegradation of vinyl chloride, cis-dichloroethene and 1,2-dichloroethane in the alkene/alkane-oxidising Mycobacterium strain NBB4. Biodegradation. 2011;22:1095–1108. doi: 10.1007/s10532-011-9466-0. PubMed DOI

Fogel MM, Taddeo AR, Fogel S. Biodegradation of chlorinated ethenes by a methane-utilizing mixed culture. Appl. Environ. Microbiol. 1986;51:720–724. PubMed PMC

Freedman DL, Danko A, Verce M. Substrate interactions during aerobic biodegradation of methane, ethene, vinyl chloride and 1,2-dichloroethenes. Water Sci. Technol. 2001;43:333–340. PubMed

Frascari D, Kim Y, Dolan ME, Semprini L. A kinetic study of aerobic propane uptake and cometabolic degradation of chloroform, cis-dichloroethylene and trichloroetylene in microcosms with groundwater/aquifer solids. Water Air Soil Pollut. 2003;3:285–298. doi: 10.1023/A:1023909229768. DOI

Kim Y, Arp DJ, Semprini L. Chlorinated solvent cometabolism by butane-grown mixed culture. J. Environ. Engineer. 2000;126:934–942. doi: 10.1061/(ASCE)0733-9372(2000)126:10(934). DOI

Ensign S, Hyman M, Arp D. Cometabolic degradation of chlorinated alkenes by alkene monooxygenase in a propylene-grown Xanthobacter strain. Appl. Environ. Microbiol. 1992;58:3038–3046. PubMed PMC

Vannelli T, Logan M, Arciero DM, Hooper AB. Degradation of halogenated aliphatic compounds by the ammonia-oxidizing bacterium Nitrosomonas europaea. Appl. Environ. Microbiol. 1990;56:1169–1171. PubMed PMC

Verce MF, Gunsch CK, Danko AS, Freedman DL. Cometabolism of cis-1,2-dichloroethene by aerobic cultures grown on vinyl chloride as the primary substrate. Environ. Sci. Technol. 2002;36:2171–2177. doi: 10.1021/es011220v. PubMed DOI

Tiehm A, Schmidt KR, Pfeifer B, Heidinger M, Ertl S. Growth kinetics and stable carbon isotope fractionation during aerobic degradation of cis-1,2-dichloroethene and vinyl chloride. Water Res. 2008;42:2431–2438. doi: 10.1016/j.watres.2008.01.029. PubMed DOI

Hopkins GD, McCarty PL. Field evaluation of in situ aerobic cometabolism of trichloroethylene and three dichloroethylene isomers using phenol and toluene as the primary substrates. Environ. Sci. Technol. 1995;29:1628–1637. doi: 10.1021/es00006a029. PubMed DOI

Elango V, Kurtz HD, Freedman DL. Aerobic cometabolism of trichloroethene and cis-dichloroethene with benzene and chlorinated benzenes as growth substrates. Chemosphere. 2011;84:247–253. doi: 10.1016/j.chemosphere.2011.04.007. PubMed DOI

Semprini L. Strategies for the aerobic co-metabolism of chlorinated solvents. Curr. Opin. Biotechnol. 1997;8:296–308. doi: 10.1016/S0958-1669(97)80007-9. PubMed DOI

Bacilio-Jiménez M, et al. Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil. 2003;249:271–277. doi: 10.1023/A:1022888900465. DOI

Bais, H. P., Broeckling, C. D. & Vivanco, J. M. in Secondary metabolites in soil ecology 241–252 (Springer, 2008).

Shukla KP, et al. Nature and role of root exudates: efficacy in bioremediation. Afr. J. Biotechnol. 2011;10:9717–9724.

Jha P, Panwar J, Jha P. Secondary plant metabolites and root exudates: guiding tools for polychlorinated biphenyl biodegradation. Int. J. Environ. Sci. Technol. 2015;12:789–802. doi: 10.1007/s13762-014-0515-1. DOI

Singer AC, Thompson IP, Bailey MJ. The tritrophic trinity: a source of pollutant-degrading enzymes and its implications for phytoremediation. Curr. Opin. Microbiol. 2004;7:239–244. doi: 10.1016/j.mib.2004.04.007. PubMed DOI

Singer AC, Crowley DE, Thompson IP. Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol. 2003;21:123–130. doi: 10.1016/S0167-7799(02)00041-0. PubMed DOI

Musilová L, Rídl J, Polívková M, Macek T, Uhlík O. Effects of Secondary Plant Metabolites on Microbial Populations: Changes in Community Structure and Metabolic Activity in Contaminated Environments. Int. J. Molec. Sci. 2016;17:1205. doi: 10.3390/ijms17081205. PubMed DOI PMC

Shim H, Ryoo D, Barbieri P, Wood T. Aerobic degradation of mixtures of tetrachloroethylene, trichloroethylene, dichloroethylenes, and vinyl chloride by toluene-o-xylene monooxygenase of Pseudomonas stutzeri OX1. Appl. Microbiol. Biotechnol. 2001;56:265–269. doi: 10.1007/s002530100650. PubMed DOI

Futamata H, Harayama S, Watanabe K. Diversity in kinetics of trichloroethylene-degrading activities exhibited by phenol-degrading bacteria. Appl. Microbiol. Biotechnol. 2001;55:248–253. doi: 10.1007/s002530000500. PubMed DOI

Rui L, Cao L, Chen W, Reardon KF, Wood TK. Active site engineering of the epoxide hydrolase from Agrobacterium radiobacter AD1 to enhance aerobic mineralization of cis-1,2-dichloroethylene in cells expressing an evolved toluene ortho-monooxygenase. J. Biol. Chem. 2004;279:46810–46817. doi: 10.1074/jbc.M407466200. PubMed DOI

Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJ. Rhizoremediation: a beneficial plant-microbe interaction. Molec. Plant-Microbe Interact. 2004;17:6–15. doi: 10.1094/MPMI.2004.17.1.6. PubMed DOI

Pham TT, Pino Rodriguez NJ, Hijri M, Sylvestre M. Optimizing Polychlorinated Biphenyl Degradation by Flavonoid-Induced Cells of the Rhizobacterium Rhodococcus erythropolis U23A. PLoS One. 2015;10:e0126033. doi: 10.1371/journal.pone.0126033. PubMed DOI PMC

Toussaint J-P, Pham T, Barriault D, Sylvestre M. Plant exudates promote PCB degradation by a rhodococcal rhizobacteria. Appl. Microbiol. Biotechnol. 2012;95:1589–1603. doi: 10.1007/s00253-011-3824-z. PubMed DOI

Siciliano SD, et al. Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl. Environ. Microbiol. 2001;67:2469–2475. doi: 10.1128/AEM.67.6.2469-2475.2001. PubMed DOI PMC

Powell CL, Agrawal A. Biodegradation of trichloroethene by methane oxidizers naturally associated with wetland plant roots. Wetlands. 2011;31:45–52. doi: 10.1007/s13157-010-0134-7. PubMed DOI

Suttinun O, Lederman PB, Luepromchai E. Application of terpene-induced cell for enhancing biodegradation of TCE contaminated soil. Songklanakarin J. Sci. Technol. 2004;26:131–142.

Gilbert ES, Crowley DE. Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl. Environ. Microbiol. 1997;63:1933–1938. PubMed PMC

Alvarez-Cohen L, Speitel GE., Jr. Kinetics of aerobic cometabolism of chlorinated solvents. Biodegradation. 2001;12:105–126. doi: 10.1023/A:1012075322466. PubMed DOI

Romantschuk M, et al. Means to improve the effect of in situ bioremediation of contaminated soil: an overview of novel approaches. Environ. Pollut. 2000;107:179–185. doi: 10.1016/S0269-7491(99)00136-0. PubMed DOI

Bacosa H, Suto K, Inoue C. Preferential degradation of aromatic hydrocarbons in kerosene by a microbial consortium. Int. Biodeter. Biodeg. 2010;64:702–710. doi: 10.1016/j.ibiod.2010.03.008. DOI

Frascari D, et al. A kinetic study of chlorinated solvent cometabolic biodegradation by propane-grown Rhodococcus sp. PB1. Biochem. Engineer. J. 2008;42:139–147. doi: 10.1016/j.bej.2008.06.011. DOI

Larkin MJ, Kulakov LA, Allen CC. Biodegradation and Rhodococcus–masters of catabolic versatility. Curr. Opin. Biotechnol. 2005;16:282–290. doi: 10.1016/j.copbio.2005.04.007. PubMed DOI

Aranda C, Godoy F, Becerra J, Barra R, Martínez M. Aerobic secondary utilization of a non-growth and inhibitory substrate 2,4,6-trichlorophenol by Sphingopyxis chilensis S37 and Sphingopyxis-like strain S32. Biodegradation. 2003;14:265–274. doi: 10.1023/A:1024752605059. PubMed DOI

Frascari D, et al. Development of an attached-growth process for the on-site bioremediation of an aquifer polluted by chlorinated solvents. Biodegradation. 2014;25:337–350. doi: 10.1007/s10532-013-9664-z. PubMed DOI

Imfeld G, et al. Characterization of microbial communities in the aqueous phase of a constructed model wetland treating 1,2-dichloroethene-contaminated groundwater. FEMS Microbiol. Ecol. 2010;72:74–88. doi: 10.1111/j.1574-6941.2009.00825.x. PubMed DOI

Clingenpeel SR, Moan JL, McGrath DM, Hungate BA, Watwood ME. Stable carbon isotope fractionation in chlorinated ethene degradation by bacteria expressing three toluene oxygenases. Front. Microbiol. 2012;3:63. doi: 10.3389/fmicb.2012.00063. PubMed DOI PMC

Lang E, Burghartz M, Spring S, Swiderski J, Spröer C. Pseudomonas benzenivorans sp. nov. and Pseudomonas saponiphila sp. nov., represented by xenobiotics degrading type strains. Curr. Microbiol. 2010;60:85–91. doi: 10.1007/s00284-009-9507-7. PubMed DOI

Ha C, et al. Natural gradient drift tests for assessing the feasibility of in situ aerobic cometabolism of trichloroethylene and evaluating the microbial community change. Water Air Soil Pollut. 2011;219:353–364. doi: 10.1007/s11270-010-0712-6. DOI

Strauch, E., Beck, S. & Appel, B. in Predatory Prokaryotes: Biology, Ecology and Evolution (ed Edouard Jurkevitch) 131–152 (Springer Berlin Heidelberg, 2007).

Fondi M, et al. The genome sequence of the hydrocarbon-degrading Acinetobacter venetianus VE-C3. Res. Microbiol. 2013;164:439–449. doi: 10.1016/j.resmic.2013.03.003. PubMed DOI

Pepi M, Minacci A, Di Cello F, Baldi F, Fani R. Long-term analysis of diesel fuel consumption in a co-culture of Acinetobacter venetianus, Pseudomonas putida and Alcaligenes faecalis. Antonie Van Leeuwenhoek. 2003;83:3–9. doi: 10.1023/A:1022930421705. PubMed DOI

Leewis MC, Uhlík O, Leigh MB. Synergistic Processing of Biphenyl and Benzoate: Carbon Flow Through the Bacterial Community in Polychlorinated-Biphenyl-Contaminated Soil. Sci. Reports. 2016;6:22145. doi: 10.1038/srep22145. PubMed DOI PMC

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951;193:265–275. PubMed

Walters W, et al. Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys. mSystems. 2016;1:e00009–00015. doi: 10.1128/mSystems.00009-15. PubMed DOI PMC

Callahan BJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Cole JR, et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014;42:D633–D642. doi: 10.1093/nar/gkt1244. PubMed DOI PMC

R Development Core Team. R: A language and environment for statistical computing (2013).

McMurdie PJ, Holmes S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE. 2013;8:e61217. doi: 10.1371/journal.pone.0061217. PubMed DOI PMC

Paulson JN, Stine OC, Bravo HC, Pop M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods. 2013;10:1200–1202. doi: 10.1038/nmeth.2658. PubMed DOI PMC

Bibi F, Ali Z. Measurement of diversity indices of avian communities at Taunsa Barrage Wildlife Sanctuary, Pakistan. J. Anim. Plant Sci. 2013;23:469–474.

Hill TC, Walsh KA, Harris JA, Moffett BF. Using ecological diversity measures with bacterial communities. FEMS Microbiol. Ecol. 2003;43:1–11. doi: 10.1111/j.1574-6941.2003.tb01040.x. PubMed DOI

Biochar-induced changes in soil microbial communities: a comparison of two feedstocks and pyrolysis temperatures

Joining the bacterial conversation: increasing the cultivation efficiency of soil bacteria with acyl-homoserine lactones and cAMP

Compost, plants and endophytes versus metal contamination: choice of a restoration strategy steers the microbiome in polymetallic mine waste

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

Prokaryotes of renowned Karlovy Vary (Carlsbad) thermal springs: phylogenetic and cultivation analysis

Genomic analysis of Acinetobacter pittii CEP14 reveals its extensive biodegradation capabilities, including cometabolic degradation of cis-1,2-dichloroethene

Soil microbial communities following 20 years of fertilization and crop rotation practices in the Czech Republic

Exploring the Potential of Micrococcus luteus Culture Supernatant With Resuscitation-Promoting Factor for Enhancing the Culturability of Soil Bacteria

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

Microbial Communities in Soils and Endosphere of Solanum tuberosum L. and their Response to Long-Term Fertilization

The stimulating role of syringic acid, a plant secondary metabolite, in the microbial degradation of structurally-related herbicide, MCPA

Whole-Cell MALDI-TOF MS Versus 16S rRNA Gene Analysis for Identification and Dereplication of Recurrent Bacterial Isolates

Complete genome sequence of Pseudomonas alcaliphila JAB1 (=DSM 26533), a versatile degrader of organic pollutants