Abstract
There is an increased interest in finding remedies for contamination in low permeability and advection-limited aquifers. A technology applicable at these sites, electrokinetic-enhanced bioremediation (EK-BIO), combines traditional bioremediation and electrokinetic technologies by applying direct current to transport bioremediation amendments and microbes in situ. The effect of this technology on the native soil microbial community has only been previously investigated at the bench scale. This research explored the influence of EK-BIO on subsurface microbial communities at a field-scale demonstration site. The results showed that, similar to the findings in laboratory studies, alpha diversity decreased and beta diversity differed temporally, based on treatment phase. Enrichments in specific taxa were linked to the bioaugmentation culture and electron donor. Overall, findings from our study, one of the first field-scale investigations of the influence of electrokinetic bioremediation on subsurface microbial communities, are very similar to bench-scale studies on the topic, suggesting good correlation between laboratory and field experiments on EK-BIO and showing that lessons learned at the benchtop are important and relevant to field-scale implementation.
Key points
• Microbial community analysis of field samples validates laboratory study results
• Bioaugmentation cultures and electron donors have largest effect on microbial community
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Raw sequences are available in the NCBI SRA under the project PRJNA637032. Other data will be available upon request to authors.
Code availability
Not applicable.
References
Acar YB, Alshawabkeh AN (1993) Principles of electrokinetic remediation. Environ Sci Technol 27:2638–2647
Asadi A, Huat BBK, Nahazanan H, Keykhah HA (2013) Theory of electroosmosis in soil. Int J Electrochem Sci 8:1016–1025
Bælum J, Scheutz C, Chambon JC, Jensen CM, Brochmann RP, Dennis P, Laier T, Broholm MM, Bjerg PL, Binning PJ, Jacobsen CS (2014) The impact of bioaugmentation on dechlorination kinetics and on microbial dechlorinating communities in subsurface clay till. Environ Pollut 186:149–157. https://doi.org/10.1016/j.envpol.2013.11.013
Battista JR (2016) Deinococcus–Thermus Group. In: eLS, John Wiley & Sons, Ltd (Ed.). https://doi.org/10.1002/9780470015902.a0021151
Bird JT, Tague ED, Zinke L, Schmidt JM, Steen AD, Reese B, Marshall IPG, Webster G, Weightman A, Castro HF, Campagna SR, Lloyd KG (2019) Uncultured microbial phyla suggest mechanisms for multi-thousand-year subsistence in baltic sea sediments. MBio 10:1–15. https://doi.org/10.1128/mBio.02376-18
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Bin KK, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, MGI L, Lee J, Ley R, Liu Y-X, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, CHD W, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Bronner G, Goss KU (2011) Sorption of organic chemicals to soil organic matter: Influence of soil variability and ph dependence. Environ Sci Technol 45:1307–1312. https://doi.org/10.1021/es102576e
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583
Canale Parola E (1977) Physiology and evolution of spirochetes. Bacteriol Rev 41:181–204. https://doi.org/10.1128/mmbr.41.1.181-204.1977
Cang L, Zhou DM, Alshawabkeh AN, Chen HF (2007) Effects of sodium hypochlorite and high pH buffer solution in electrokinetic soil treatment on soil chromium removal and the functional diversity of soil microbial community. J Hazard Mater 142:111–117. https://doi.org/10.1016/j.jhazmat.2006.07.067
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516 LP–4514522. https://doi.org/10.1073/pnas.1000080107
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8
Chen LX, Méndez-García C, Dombrowski N, Servín-Garcidueñas LE, Eloe-Fadrosh EA, Fang BZ, Luo ZH, Tan S, Zhi XY, Hua ZS, Martinez-Romero E, Woyke T, Huang LN, Sánchez J, Peláez AI, Ferrer M, Baker BJ, Shu WS (2018) Metabolic versatility of small archaea Micrarchaeota and Parvarchaeota. ISME J 12:756–775. https://doi.org/10.1038/s41396-017-0002-z
Cox E, Wang J, Reynolds D, Gent D, Singletary M, Wilson A (2018) Electrokinetic-Enhanced (EK-enhanced) Amendment Delivery for Remediation of Low Permeability and Heterogeneous Materials. Report ESTCP ER-201325, ESTCP: Alexandria
Doronina N, Kaparullina E, Trotsenko Y (2014) The family Methylophilaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: alphaproteobacteria and betaproteobacteria. Springer, Berlin Heidelberg, pp 869–880
Garrity GM, Bell JA, Lilburn T (2005) In: Brenner DJ, Krieg NR, Staley JT (eds) Class II. Betaproteobacteria class. nov. BT - Bergey’s Manual® of systematic bacteriology: volume two the proteobacteria part c the alpha-, beta-, delta-, and epsilonproteobacteria. Springer US, Boston, pp 575–922
Gill RT, Harbottle MJ, Smith JWN, Thornton SF (2014) Electrokinetic-enhanced bioremediation of organic contaminants: a review of processes and environmental applications. Chemosphere 107:31–42. https://doi.org/10.1016/j.chemosphere.2014.03.019
Guo S, Fan R, Li T, Hartog N, Li F, Yang X (2014) Synergistic effects of bioremediation and electrokinetics in the remediation of petroleum-contaminated soil. Chemosphere 109:226–233. https://doi.org/10.1016/j.chemosphere.2014.02.007
Handley KM, Wrighton KC, Miller CS, Wilkins MJ, Kantor RS, Thomas BC, Williams KH, Gilbert JA, Long PE, Banfield JF (2015) Disturbed subsurface microbial communities follow equivalent trajectories despite different structural starting points. Environ Microbiol 17:622–636. https://doi.org/10.1111/1462-2920.12467
He J, Sung Y, Krajmalnik-Brown R, Ritalahti KM, Löffler FE (2005) Isolation and characterization of Dehalococcoides sp. strain FL2, a trichloroethene (TCE)- and 1,2-dichloroethene-respiring anaerobe. Environ Microbiol 7:1442–1450. https://doi.org/10.1111/j.1462-2920.2005.00830.x
Hiller KA, Foreman KH, Weisman D, Bowen JL (2015) Permeable reactive barriers designed to mitigate eutrophication alter bacterial community composition and aquifer redox conditions. Appl Environ Microbiol 81:7114–7124. https://doi.org/10.1128/AEM.01986-15
Huang W, Chen X, Jiang X, Zheng B (2017) Characterization of sediment bacterial communities in plain lakes with different trophic statuses. Microbiologyopen 6:1–14. https://doi.org/10.1002/mbo3.503
Kang D-W, Adams JB, Coleman DM, Pollard EL, Maldonado J, McDonough-Means S, Caporaso JG, Krajmalnik-Brown R (2019) Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota. Sci Rep 9:5821. https://doi.org/10.1038/s41598-019-42183-0
Kao C-M, Liao H-Y, Chien C-C, Tseng Y-K, Tang P, Lin C-E, Chen S-C (2016) The change of microbial community from chlorinated solvent-contaminated groundwater after biostimulation using the metagenome analysis. J Hazard Mater 302:144–150. https://doi.org/10.1016/j.jhazmat.2015.09.047
Kim SH, Han HY, Lee YJ, Kim CW, Yang JW (2010) Effect of electrokinetic remediation on indigenous microbial activity and community within diesel contaminated soil. Sci Total Environ 408:3162–3168. https://doi.org/10.1016/j.scitotenv.2010.03.038
Lear G, Harbottle MJ, Van Der Gast CJ, Jackman SA, Knowles CJ, Sills G, Thompson IP (2004) The effect of electrokinetics on soil microbial communities. Soil Biol Biochem 36:1751–1760. https://doi.org/10.1016/j.soilbio.2004.04.032
Lear G, Harbottle MJ, Sills G, Knowles CJ, Semple KT, Thompson IP (2007) Impact of electrokinetic remediation on microbial communities within PCP contaminated soil. Environ Pollut 146:139–146. https://doi.org/10.1016/j.envpol.2006.06.037
Li H, Li B, Zhang Z, Zhu C, Tian Y, Ye J (2018) Evolution of microbial communities during electrokinetic treatment of antibiotic-polluted soil. Ecotoxicol Environ Saf 148:842–850. https://doi.org/10.1016/j.ecoenv.2017.11.057
Mao X, Wang J, Ciblak A, Cox EE, Riis C, Terkelsen M, Gent DB, Alshawabkeh AN (2012) Electrokinetic-enhanced bioaugmentation for remediation of chlorinated solvents contaminated clay. J Hazard Mater 213–214:311–317. https://doi.org/10.1016/j.jhazmat.2012.02.001
Mayorga OL, Kingston-Smith AH, Kim EJ, Allison GG, Wilkinson TJ, Hegarty MJ, Theodorou MK, Newbold CJ, Huws SA (2016) Temporal metagenomic and metabolomic characterization of fresh perennial ryegrass degradation by rumen bacteria. Front Microbiol 7:1–23. https://doi.org/10.3389/fmicb.2016.01854
Nelson WC, Stegen JC (2015) The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle. Front Microbiol 6:1–14. https://doi.org/10.3389/fmicb.2015.00713
Nemir A, David MM, Perrussel R, Sapkota A, Simonet P, Monier JM, Vogel TM (2010) Comparative phylogenetic microarray analysis of microbial communities in TCE-contaminated soils. Chemosphere 80:600–607. https://doi.org/10.1016/j.chemosphere.2010.03.036
Ormerod KL, Wood DLA, Lachner N, Gellatly SL, Daly JN, Parsons JD, Dal’Molin CGO, Palfreyman RW, Nielsen LK, Cooper MA, Morrison M, Hansbro PM, Hugenholtz P (2016) Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals. Microbiome 4:1–17. https://doi.org/10.1186/s40168-016-0181-2
Paul S, Cortez Y, Vera N, Villena G, Gutiérrez-Correa M (2016) Metagenomic analysis of microbial communities in the soil-mousse surrounding of an Amazonian geothermal spring in Peru. Br Biotechnol J 15:1–11
Plugge CM, Zhang W, Scholten JCM, Stams AJM (2011) Metabolic flexibility of sulfate-reducing bacteria. Front Microbiol 2:1–8. https://doi.org/10.3389/fmicb.2011.00081
Qu JH, Yuan HL (2008) Sediminibacterium salmoneum gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from sediment of a eutrophic reservoir. Int J Syst Evol Microbiol 58:2191–2194. https://doi.org/10.1099/ijs.0.65514-0
Siezen RJ, Tzeneva VA, Castioni A, Wels M, Phan HTK, Rademaker JLW, Starrenburg MJC, Kleerebezem M, van Hylckama Vlieg JET (2010) Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ Microbiol 12:758–773. https://doi.org/10.1111/j.1462-2920.2009.02119.x
Suni S, Romantschuk M (2004) Mobilisation of bacteria in soils by electro-osmosis. FEMS Microbiol Ecol 49:51–57. https://doi.org/10.1016/j.femsec.2004.01.016
Wan C, Du M, Lee DJ, Yang X, Ma W, Zheng L (2011) Electrokinetic remediation and microbial community shift of β-cyclodextrin-dissolved petroleum hydrocarbon-contaminated soil. Appl Microbiol Biotechnol 89:2019–2025. https://doi.org/10.1007/s00253-010-2952-1
Wang QY, Zhou DM, Cang L, Li LZ, Wang P (2009) Solid/solution Cu fractionations/speciation of a Cu contaminated soil after pilot-scale electrokinetic remediation and their relationships with soil microbial and enzyme activities. Environ Pollut 157:2203–2208. https://doi.org/10.1016/j.envpol.2009.04.013
Wick LY, Mattle PA, Wattiau P, Harms H (2004) Electrokinetic transport of PAH-degrading bacteria in model aquifers and soil. Environ Sci Technol 38:4596–4602. https://doi.org/10.1021/es0354420
Wick LY, Buchholz F, Fetzer I, Kleinsteuber S, Härtig C, Shi L, Miltner A, Harms H, Pucci GN (2010) Responses of soil microbial communities to weak electric fields. Sci Total Environ 408:4886–4893. https://doi.org/10.1016/j.scitotenv.2010.06.048
Willems A, De Ley J, Gillis M, Kersters K (1991) Comamonadaceae, a new family encompassing the acidovorans. Int J Syst Bacteriol 41:445–450
Wu X, Gent DB, Davis JL, Alshawabkeh AN (2012) Lactate injection by electric currents for bioremediation of tetrachloroethylene in clay. Electrochim Acta 86:157–163. https://doi.org/10.1016/j.electacta.2012.06.046
Zhao X, Kuipers OP (2016) Identification and classification of known and putative antimicrobial compounds produced by a wide variety of Bacillales species. BMC Genomics 17:1–18. https://doi.org/10.1186/s12864-016-3224-y
Ziv-El M, Popat SC, Parameswaran P, Kang DW, Polasko A, Halden RU, Rittmann BE, Krajmalnik-Brown R (2012) Using electron balances and molecular techniques to assess trichoroethene-induced shifts to a dechlorinating microbial community. Biotechnol Bioeng 109:2230–2239. https://doi.org/10.1002/bit.24504
Acknowledgements
Field samples and associated geochemical data used in this work were provided by the Geosyntec Consultants, Inc., from its EK-BIO project funded by the Department of Defense Environmental Security and Technology Certification Program (ESTCP) Project ER-201325.
Funding
This study was funded by the National Science Foundation (NSF) under NSF Award Number ERC-1449501 and the Arizona State University (ASU) Dean’s Fellowship.
Author information
Authors and Affiliations
Contributions
MA performed microbial ecology analysis and prepared a draft of the manuscript under the guidance of RKB and CT. PD, JW, and EC provided samples for analysis and edited the manuscript. All authors read and approved of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflicts of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Meinel, M., Wang, J., Cox, E. et al. The influence of electrokinetic bioremediation on subsurface microbial communities at a perchloroethylene contaminated site. Appl Microbiol Biotechnol 105, 6489–6497 (2021). https://doi.org/10.1007/s00253-021-11458-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-021-11458-w