Skip to main content

Advertisement

Log in

Surfactant-induced bacterial community changes correlated with increased polycyclic aromatic hydrocarbon degradation in contaminated soil

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Bioremediation as a method for removing polycyclic aromatic hydrocarbons (PAHs) from contaminated environments has been criticized for poor removal of potentially carcinogenic but less bioavailable high molecular weight (HMW) compounds. As a partial remedy to this constraint, we studied surfactant addition at sub-micellar concentrations to contaminated soil to enhance the biodegradation of PAHs remaining after conventional aerobic bioremediation. We demonstrated increased removal of four- and five-ring PAHs using two nonionic surfactants, polyoxyethylene(4)lauryl ether (Brij 30) and polyoxyethylene sorbitol hexaoleate (POESH), and analyzed bacterial community shifts associated with those conditions. Eight groups of abundant bacteria were implicated as potentially being involved in increased HMW PAH removal. A group of unclassified Alphaproteobacteria and members of the Phenylobacterium genus in particular showed significantly increased relative abundance in the two conditions exhibiting increased PAH removal. Other implicated groups included members of the Sediminibacterium, Terrimonas, Acidovorax, and Luteimonas genera, as well as uncharacterized organisms within the families Chitinophagaceae and Bradyrhizobiaceae. Targeted isolation identified a subset of the community likely using the surfactants as a growth substrate, but few of the isolates exhibited PAH-degradation capability. Isolates recovered from the Acidovorax and uncharacterized Bradyrhizobiaceae groups suggest the abundance of those groups may have been attributable to growth on surfactants. Understanding the specific bacteria responsible for HMW PAH removal in natural and engineered systems and their response to stimuli such as surfactant amendment may improve bioremediation efficacy during treatment of contaminated environmental media.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adrion AC, Nakamura J, Shea D, Aitken MD (2016) Screening nonionic surfactants for enhanced biodegradation of polycyclic aromatic hydrocarbons remaining in soil after conventional biological treatment. Environ Sci Technol 50:3838–3845

    Article  CAS  PubMed  Google Scholar 

  • Agency for Toxic Substances and Disease Registry (2015) Priority List of Hazardous Substances. ATSDR. Accessed 4/21/16

  • Ahn TS, Lee GH, Song HG (2005) Biodegradation of phenanthrene by psychrotrophic bacteria from Lake Baikal. J Microbiol Biotechnol 15:1135–1139

    CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bacosa HP, Inoue C (2015) Polycyclic aromatic hydrocarbons (PAHs) biodegradation potential and diversity of microbial consortia enriched from tsunami sediments in Miyagi, Japan. J Hazard Mater 283:689–697

    Article  CAS  PubMed  Google Scholar 

  • Boonchan S, Britz ML, Stanley GA (1998) Surfactant-enhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia. Biotechnol Bioeng 59:482–494

    Article  CAS  PubMed  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST plus : architecture and applications. BMC Bioinformatics 10:421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cerniglia CE (1993) Biodegradation of polycyclic aromatic hydrocarbons. Curr Opin Biotechnol 4:331–338

    Article  CAS  Google Scholar 

  • Chang Y-T, Hung C-H, Chou H-L (2014) Effects of polyethoxylate lauryl ether (Brij 35) addition on phenanthrene biodegradation in a soil/water system. J Environ Sci Health, Part A 49:1672–1684

    Article  CAS  Google Scholar 

  • Chen P, Pickard M, Gray M (2000) Surfactant inhibition of bacterial growth on solid anthracene. Biodegradation 11:341–347

    Article  CAS  PubMed  Google Scholar 

  • Churchill SA, Griffin RA, Jones LP, Churchill PF (1995) Biodegradation rate enhancement of hydrocarbons by an oleophilic fertilizer and a rhamnolipid biosurfactant. J Environ Qual 24:19–28

    Article  CAS  Google Scholar 

  • Ding GC, Heuer H, Smalla K (2012) Dynamics of bacterial communities in two unpolluted soils after spiking with phenanthrene: soil type specific and common responders. Front Microbiol 3:290

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong J, Chowdhry B, Leharne S (2004) Investigation of the wetting behavior of coal tar in three phase systems and its modification by poloxamine block copolymeric surfactants. Environ Sci Technol 38:594–602

    Article  CAS  PubMed  Google Scholar 

  • Doong RA, Lei WG (2003) Solubilization and mineralization of polycyclic aromatic hydrocarbons by Pseudomonas putida in the presence of surfactant. J Hazard Mater 96:15–27

    Article  CAS  PubMed  Google Scholar 

  • Elliot R, Singhal N, Swift S (2010) Surfactants and bacterial bioremediation of polycyclic aromatic hydrocarbon contaminated soil—unlocking the targets. Crit Rev Environ Sci Technol 41:78–124

    Article  CAS  Google Scholar 

  • Frutos FJG, Escolano O, García S, Ivey GA (2011) Mobilization assessment and possibility of increased availability of PAHs in contaminated soil using column tests. Soil Sediment Contam 20:581–591

    Article  CAS  Google Scholar 

  • Gan S, Lau EV, Ng HK (2009) Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172:532–549

    Article  CAS  PubMed  Google Scholar 

  • Guha S, Jaffé PR (1996) Biodegradation kinetics of phenanthrene partitioned into the micellar phase of nonionic surfactants. Environ Sci Technol 30:605–611

    Article  CAS  Google Scholar 

  • Hu J, Nakamura J, Richardson SD, Aitken MD (2012) Evaluating the effects of bioremediation on genotoxicity of polycyclic aromatic hydrocarbon-contaminated soil using genetically engineered, higher eukaryotic cell lines. Environ Sci Technol 46:4607–4613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jahan K, Ahmed T, Maier WJ (1997) Factors affecting the nonionic surfactant-enhanced biodegradation of phenanthrene. Water Environ Res 69:317–325

    Article  CAS  Google Scholar 

  • Jin D, Jiang X, Jing X, Ou Z (2007) Effects of concentration, head group, and structure of surfactants on the degradation of phenanthrene. J Hazard Mater 144:215–221

    Article  CAS  PubMed  Google Scholar 

  • Jones MD, Singleton DR, Carstensen DP, Powell SN, Swanson JS, Pfaender FK, Aitken MD (2008) Effect of incubation conditions on the enrichment of pyrene-degrading bacteria identified by stable-isotope probing in an aged, PAH-contaminated soil. Microb Ecol 56:341–349

    Article  CAS  PubMed  Google Scholar 

  • Jones MD, Crandell DW, Singleton DR, Aitken MD (2011) Stable-isotope probing of the polycyclic aromatic hydrocarbon-degrading bacterial guild in a contaminated soil. Environ Microbiol 13:2623–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones MD, Rodgers-Vieira EA, Hu J, Aitken MD (2014) Association of growth substrates and bacterial genera with benzo[a]pyrene mineralization in contaminated soil. Environ Eng Sci 31:689–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kile DE, Chiou CT (1989) Water solubility enhancements of DDT and trichlorobenzene by some surfactants below and above the critical micelle concentration. Environ Sci Technol 23:832–838

    Article  CAS  Google Scholar 

  • Kim M, Kang O, Zhang Y, Ren L, Chang X, Jiang F, Fang C, Zheng C, Peng F (2016) Sphingoaurantiacus polygranulatus gen. nov., sp. nov., isolated from high-Arctic tundra soil, and emended descriptions of the genera Sandarakinorhabdus, Polymorphobacter and Rhizorhabdus and the species Sandarakinorhabdus limnophila, Rhizorhabdus argentea and Sphingomonas wittichii. Int J Syst Evol Microbiol 66:91–100

    Article  CAS  PubMed  Google Scholar 

  • Kojima H, Fukui M (2011) Sulfuritalea hydrogenivorans gen. nov., sp. nov., a facultative autotroph isolated from a freshwater lake. Int J Syst Evol Microbiol 61:1651–1655

    Article  CAS  PubMed  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol

  • Li J-L, Chen B-H (2009) Surfactant-mediated biodegradation of polycyclic aromatic hydrocarbons. Materials 2:76–94

    Article  CAS  Google Scholar 

  • Liu ZB, Jacobson AM, Luthy RG (1995) Biodegradation of naphthalene in aqueous nonionic surfactant systems. Appl Environ Microbiol 61:145–151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lladó S, Solanas AM, de Lapuente J, Borràs M, Viñas M (2012) A diversified approach to evaluate biostimulation and bioaugmentation strategies for heavy-oil-contaminated soil. Sci Total Environ 435–436:262–269

    Article  CAS  PubMed  Google Scholar 

  • Lladó S, Covino S, Solanas AM, Vinas M, Petruccioli M, D’Annibale A (2013) Comparative assessment of bioremediation approaches to highly recalcitrant PAH degradation in a real industrial polluted soil. J Hazard Mater 248-249:407–414

    Article  CAS  PubMed  Google Scholar 

  • Lladó S, Covino S, Solanas AM, Petruccioli M, D’annibale A, Viñas M (2015) Pyrosequencing reveals the effect of mobilizing agents and lignocellulosic substrate amendment on microbial community composition in a real industrial PAH-polluted soil. J Hazard Mater 283:35–43

    Article  CAS  PubMed  Google Scholar 

  • Makkar RS, Rockne KJ (2003) Comparison of synthetic surfactants and biosurfactants in enhancing biodegradation of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 22:2280–2292

    Article  CAS  PubMed  Google Scholar 

  • May WE, Wasik SP, Freeman DH (1978) Determination of the solubility behavior of some polycyclic aromatic hydrocarbons in water. Anal Chem 50:997–1000

    Article  CAS  Google Scholar 

  • National Toxicology Program (2014) Report on carcinogens, thirteenth edition. U.S. Department of Health and Human Services Public Health Service. Research Triangle Park, NC

  • Noordman WH, Bruining J-W, Wietzes P, Janssen DB (2000) Facilitated transport of a PAH mixture by a rhamnolipid biosurfactant in porous silica matrices. J Contam Hydrol 44:119–140

    Article  CAS  Google Scholar 

  • Núñez EV, Valenzuela-Encinas C, Alcántara-Hernández RJ, Navarro-Noya YE, Luna-Guido M, Marsch R, Dendooven L (2012) Modifications of bacterial populations in anthracene contaminated soil. Appl Soil Ecol 61:113–126

    Article  Google Scholar 

  • Oggerin M, Arahal DR, Rubio V, Marin I (2009) Identification of Beijerinckia fluminensis strains CIP 106281T and UQM 1685T as Rhizobium radiobacter strains, and proposal of Beijerinckia doebereinerae sp. nov. to accommodate Beijerinckia fluminensis LMG 2819. Int J Syst Evol Microbiol 59:2323–2328

    Article  CAS  PubMed  Google Scholar 

  • O’Neill B, Grossman J, Tsai MT, Gomes JE, Lehmann J, Peterson J, Neves E, Thies JE (2009) Bacterial community composition in Brazilian Anthrosols and adjacent soils characterized using culturing and molecular identification. Microb Ecol 58:23–35

    Article  PubMed  Google Scholar 

  • Pantsyrnaya T, Blanchard F, Delaunay S, Goergen JL, Guedon E, Guseva E, Boudrant J (2011) Effect of surfactants, dispersion and temperature on solubility and biodegradation of phenanthrene in aqueous media. Chemosphere 83:29–33

    Article  CAS  PubMed  Google Scholar 

  • Pantsyrnaya T, Delaunay S, Goergen JL, Guedon E, Paris C, Poupin P, Guseva E, Boudrant J (2012) Biodegradation of phenanthrene by Pseudomonas putida and a bacterial consortium in the presence and in the absence of a surfactant. Indian J Microbiol 52:420–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peeters K, Hodgson DA, Convey P, Willems A (2011) Culturable diversity of heterotrophic bacteria in Forlidas Pond (Pensacola Mountains) and Lundstrom Lake (Shackleton Range), Antarctica. Microb Ecol 62:399–413

    Article  PubMed  Google Scholar 

  • Richardson SD, Aitken MD (2011) Desorption and bioavailability of polycyclic aromatic hydrocarbons in contaminated soil subjected to long-term in situ biostimulation. Environ Toxicol Chem 30:2674–2681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson SD, Lebron B, Miller CT, Aitken MD (2011) Recovery of phenanthrene-degrading bacteria after simulated in situ persulfate oxidation in contaminated soil. Environ Sci Technol 45:719–725

    Article  CAS  PubMed  Google Scholar 

  • Rodgers-Vieira EA, Zhang Z, Adrion AC, Gold A, Aitken MD (2015) Identification of anthraquinone-degrading bacteria in soil contaminated with polycyclic aromatic hydrocarbons. Appl Environ Microbiol 81:3775–3781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singleton DR, Powell SN, Sangaiah R, Gold A, Ball LM, Aitken MD (2005) Stable-isotope probing of bacteria capable of degrading salicylate, naphthalene, or phenanthrene in a bioreactor treating contaminated soil. Appl Environ Microbiol 71:1202–1209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singleton DR, Sangaiah R, Gold A, Ball LM, Aitken MD (2006) Identification and quantification of uncultivated Proteobacteria associated with pyrene degradation in a bioreactor treating PAH-contaminated soil. Environ Microbiol 10:1736–1745

    Article  CAS  Google Scholar 

  • Singleton DR, Hunt M, Powell SN, Frontera-Suau R, Aitken MD (2007) Stable-isotope probing with multiple growth substrates to determine substrate specificity of uncultivated bacteria. J Microbiol Methods 69:180–187

    Article  CAS  PubMed  Google Scholar 

  • Singleton DR, Ramirez LG, Aitken MD (2009) Characterization of a polycyclic aromatic hydrocarbon degradation gene cluster in a phenanthrene-degrading Acidovorax strain. Appl Environ Microbiol 75:2613–2620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singleton DR, Richardson SD, Aitken MD (2011) Pyrosequence analysis of bacterial communities in aerobic bioreactors treating polycyclic aromatic hydrocarbon-contamined soil. Biodegradation 22:1061–1073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song M, Luo C, Jiang L, Zhang D, Wang Y, Zhang G (2015) Identification of benzo[a]pyrene-metabolizing bacteria in forest soils by using DNA-based stable-isotope probing. Appl Environ Microbiol 81:7368–7376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stelmack PL, Gray MR, Pickard MA (1999) Bacterial adhesion to soil contaminants in the presence of surfactants. Appl Environ Microbiol 65:163–168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tauler M, Vila J, Nieto JM, Grifoll M (2016) Key high molecular weight PAH-degrading bacteria in a soil consortium enriched using a sand-in-liquid microcosm system. Appl Microbiol Biotechnol 100:3321–3336

    Article  CAS  PubMed  Google Scholar 

  • Tejeda-Agredano MC, Gallego S, Vila J, Grifoll M, Ortega-Calvo JJ, Cantos M (2013) Influence of the sunflower rhizosphere on the biodegradation of PAHs in soil. Soil Biol Biochem 57:830–840

    Article  CAS  Google Scholar 

  • Thomas F, Cébron A (2016) Short-term rhizosphere effect on available carbon sources, phenanthrene degradation and active microbiome in an aged-contaminated industrial soil. Frontiers in Microbiology 7

  • Tiehm A (1994) Degradation of polycyclic aromatic hydrocarbons in the presence of synthetic surfactants. Appl Environ Microbiol 60:258–263

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tiehm A, Stieber M, Werner P, Frimmel FH (1997) Surfactant-enhanced mobilization and biodegradation of polycyclic aromatic hydrocarbons in manufactured gas plant soil. Environ Sci Technol 31:2570–2576

    Article  CAS  Google Scholar 

  • U. S. Environmental Protection Agency (2007) Treatment technologies for site cleanup: annual status report. Washington, DC

  • Volkering F, Breure AM, Rulkens WH (1997) Microbiological aspects of surfactant use for biological soil remediation. Biodegradation 8:401–417

    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 

  • White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comp Biol 5:e1000352

    Article  CAS  Google Scholar 

  • Yeom IT, Ghosh MM, Cox CD (1996) Kinetic aspects of surfactant solubilization of soil-bound polycyclic aromatic hydrocarbons. Environ Sci Technol 30:1589–1595

    Article  CAS  Google Scholar 

  • Yessica G-P, Alejandro A, Ronald F-C, José AJ, Esperanza M-R, Samuel C-SJ, Remedios M-LM, Ormeño-Orrillo E (2013) Tolerance, growth and degradation of phenanthrene and benzo[a]pyrene by Rhizobium tropici CIAT 899 in liquid culture medium. Appl Soil Ecol 63:105–111

    Article  Google Scholar 

  • Yuan SY, Wei SH, Chang BV (2000) Biodegradation of polycyclic aromatic hydrocarbons by a mixed culture. Chemosphere 41:1463–1468

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Miller RM (1992) Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant). Appl Environ Microbiol 58:3276–3282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S-Y, Wang Q-F, Wan R, Xie S-G (2011) Changes in bacterial community of anthracene bioremediation in municipal solid waste composting soil. J Zhejiang Univ Sci B 12:760–768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao HP, Wu QS, Wang L, Zhao XT, Gao HW (2009) Degradation of phenanthrene by bacterial strain isolated from soil in oil refinery fields in Shanghai China. J Hazard Mater 164:863–869

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Aitken MD (2010) Surfactant-enhanced desorption and biodegradation of polycyclic aromatic hydrocarbons in contaminated soil. Environ Sci Technol 44:7260–7265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu H, Singleton D, Aitken M (2010) Effects of nonionic surfactant addition on populations of polycyclic aromatic hydrocarbon-degrading bacteria in contaminated soil. Environ Sci Technol 19:7266–7271

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David R. Singleton.

Ethics declarations

Funding

This work was funded by the U.S. National Institute of Environmental Health Sciences (NIEHS) Superfund Research Program (grant P42 ES005948).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Electronic supplementary material

ESM 1

(PDF 167 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singleton, D.R., Adrion, A.C. & Aitken, M.D. Surfactant-induced bacterial community changes correlated with increased polycyclic aromatic hydrocarbon degradation in contaminated soil. Appl Microbiol Biotechnol 100, 10165–10177 (2016). https://doi.org/10.1007/s00253-016-7867-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7867-z

Keywords

Navigation