Skip to main content
SpringerLink
Log in

The impact of calcium peroxide on groundwater bacterial diversity during naphthalene removal by permeable reactive barrier (PRB)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Oxygen-releasing compounds (ORCs) have recently gained much attention in contaminated groundwater remediation. We investigated the impact of calcium peroxide nanoparticles on the groundwater indigenous bacteria in a bioremediation process by permeable reactive barrier (PRB). Three sand-packed columns were applied, including (1) control column (fresh groundwater), (2) natural remediation column (contaminated groundwater), and (3) biostimulation column (contaminated groundwater amended with CaO2). Actinobacteria and Proteobacteria constituted the main phyla among the identified isolates. According to the results of next-generation sequencing, Proteobacteria was the dominant phylum (81% relative abundance) in the natural remediation condition. But, it was declined to 38.1% in the biostimulation column. Meanwhile, the abundance of Actinobacteria and Bacteroidetes were increased to 25.9% and 15.4%, respectively, by exposing the groundwater microbial structure to CaO2 nanoparticles. Furthermore, orders Chlamydiales, Nitrospirales, and Oceanospirillales existing in the control column were detected in the presence of naphthalene. Shannon index was 4.32 for the control column samples, while it was reduced to 2.73 and 2.00 in the natural and biostimulation columns, respectively. Therefore, the present study provides a considerable insight into the impact of ORCs on the groundwater microbial community during the bioremediation process.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abed RM, Safi NM, Köster J, De Beer D, El-Nahhal Y, Rullkötter J, Garcia-Pichel F (2002) Microbial diversity of a heavily polluted microbial mat and its community changes following degradation of petroleum compounds. Appl Environ Microbiol 68:1674–1683

    Article  CAS  Google Scholar 

  • Backman A, Jansson JK (2004) Degradation of 4-chlorophenol at low temperature and during extreme temperature fluctuations by Arthrobacter chlorophenolicus A6. Microb Ecol 48:246–253

    Article  CAS  Google Scholar 

  • Barman SR, Banerjee P, Mukhopadhayay A, Das P (2017) Biodegradation of acenapthene and naphthalene by Pseudomonas mendocina: Process optimization, and toxicity evaluation. J Environ Chem Eng 5:4803–4812

    Article  CAS  Google Scholar 

  • Behera BK, Das A, Sarkar DJ, Weerathunge P, Parida PK, Das BK, Thavamani P, Ramanathan R, Bansal V (2018) Polycyclic aromatic hydrocarbons (PAHs) in inland aquatic ecosystems: perils and remedies through biosensors and bioremediation. Environ Pollut 241:212–233

    Article  CAS  Google Scholar 

  • Blázquez B, Carmona M, Díaz E (2018) Transcriptional regulation of the peripheral pathway for the anaerobic catabolism of toluene and m-xylene in Azoarcus sp. CIB. Front Microbiol 9:506

    Article  Google Scholar 

  • Chaudhary P, Sahay H, Sharma R, Pandey AK, Singh SB, Saxena AK, Nain L (2015) Identification and analysis of polyaromatic hydrocarbons (PAHs)—biodegrading bacterial strains from refinery soil of India. Environ Monit Assess 187:391. https://doi.org/10.1007/s10661-015-4617-0

    Article  CAS  Google Scholar 

  • Cheng W, Zhang J, Wang Z, Wang M, Xie S (2014) Bacterial communities in sediments of a drinking water reservoir. Ann Microbiol 64:875–878

    Article  CAS  Google Scholar 

  • Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2001) Isolation of bacteria and 16S rDNAs from Lake Vostok accretion ice. Environ Microbiol 3:570–577

    Article  CAS  Google Scholar 

  • Colombo M, Cavalca L, Bernasconi S, Andreoni V (2011) Bioremediation of polyaromatic hydrocarbon contaminated soils by native microflora and bioaugmentation with Sphingobium chlorophenolicum strain C3R: a feasibility study in solid-and slurry-phase microcosms. Int Biodeterior Biodegradation 65:191–197

    Article  CAS  Google Scholar 

  • Cupples AM (2013) RDX degrading microbial communities and the prediction of microorganisms responsible for RDX bioremediation. Int Biodeterior Biodegradation 85:260–270

    Article  CAS  Google Scholar 

  • Di Gennaro P, Rescalli E, Galli E, Sello G, Bestetti G (2001) Characterization of Rhodococcus opacus R7, a strain able to degrade naphthalene and o-xylene isolated from a polycyclic aromatic hydrocarbon-contaminated soil. Res Microbiol 152:641–651

    Article  Google Scholar 

  • Di Gennaro P, Terreni P, Masi G, Botti S, De Ferra F, Bestetti G (2010) Identification and characterization of genes involved in naphthalene degradation in Rhodococcus opacus R7. Appl Microbiol Biotechnol 87:297–308

    Article  CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996

    Article  CAS  Google Scholar 

  • Fahy A, Lethbridge G, Earle R, Ball AS, Timmis KN, McGenity TJ (2005) Effects of long-term benzene pollution on bacterial diversity and community structure in groundwater. Environ Microbiol 7:1192–1199

    Article  CAS  Google Scholar 

  • Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98:4781–4794

    Article  CAS  Google Scholar 

  • Gawor J, Grzesiak J, Sasin-Kurowska J, Borsuk P, Gromadka R, Górniak D, Świątecki A, Aleksandrzak-Piekarczyk T, Zdanowski MK (2016) Evidence of adaptation, niche separation and microevolution within the genus Polaromonas on Arctic and Antarctic glacial surfaces. Extremophiles 20:403–413

    Article  Google Scholar 

  • Gholami F, Shavandi M, Dastgheib SMM, Amoozegar MA (2018) Naphthalene remediation from groundwater by calcium peroxide (CaO2) nanoparticles in permeable reactive barrier (PRB). Chemosphere 212:105–113. https://doi.org/10.1016/j.chemosphere.2018.08.056

    Article  CAS  Google Scholar 

  • Gholami F, Mosmeri H, Shavandi M, Dastgheib SMM, Amoozegar MA (2019) Application of encapsulated magnesium peroxide (MgO2) nanoparticles in permeable reactive barrier (PRB) for naphthalene and toluene bioremediation from groundwater. Sci Total Environ 655:633–640

    Article  CAS  Google Scholar 

  • Goldman R, Enewold L, Pellizzari E, Beach JB, Bowman ED, Krishnan SS, Shields PG (2001) Smoking increases carcinogenic polycyclic aromatic hydrocarbons in human lung tissue. Cancer Res 61:6367–6371

    CAS  Google Scholar 

  • Hanapiah M, Zulkifli SZ, Mustafa M, Mohamat-Yusuff F, Ismail A (2018) Isolation, characterization, and identification of potential Diuron-degrading bacteria from surface sediments of Port Klang, Malaysia. Mar Pollut Bull 127:453–457

    Article  CAS  Google Scholar 

  • Jeon CO, Park W, Ghiorse WC, Madsen EL (2004) Polaromonas naphthalenivorans sp. nov., a naphthalene-degrading bacterium from naphthalene-contaminated sediment. Int J Syst Evol Microbiol 54:93–97

    Article  CAS  Google Scholar 

  • Jin J, Wu G, Guan Y (2015) Effect of bacterial communities on the formation of cast iron corrosion tubercles in reclaimed water. Water Res 71:207–218

    Article  CAS  Google Scholar 

  • Kaszab E, Kriszt B, Atzél B, Szabó G, Szabó I, Harkai P, Szoboszlay S (2010) The occurrence of multidrug-resistant Pseudomonas aeruginosa on hydrocarbon-contaminated sites. Microb Ecol 59:37–45

    Article  CAS  Google Scholar 

  • Kertesz MA, Kawasaki A (2010) Hydrocarbon-degrading Sphingomonads: Sphingomonas, Sphingobium, Novosphingobium, and Sphingopyxis. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 1693–1705. https://doi.org/10.1007/978-3-540-77587-4_119

    Chapter  Google Scholar 

  • Lee DW, Lee H, Lee AH, Kwon BO, Khim JS, Yim UH, Kim BS, Kim JJ (2018) Microbial community composition and PAHs removal potential of indigenous bacteria in oil contaminated sediment of Taean coast, Korea. Environ Pollut 234:503–512

    Article  CAS  Google Scholar 

  • Lhotský O et al (2017) Assessment of biodegradation potential at a site contaminated by a mixture of BTEX, chlorinated pollutants and pharmaceuticals using passive sampling methods–case study. Sci Total Environ 607:1451–1465

    Article  CAS  Google Scholar 

  • Liu Y, Zhang J, Zhao L, Zhang X, Xie S (2014) Spatial distribution of bacterial communities in high-altitude freshwater wetland sediment. Limnology 15:249–256

    Article  Google Scholar 

  • Lors C, Damidot D, Ponge J-F, Périé F (2012) Comparison of a bioremediation process of PAHs in a PAH-contaminated soil at field and laboratory scales. Environ Pollut 165:11–17

    Article  CAS  Google Scholar 

  • Lowa WL, Leea C, Wilkesa M, Robertsb C, Hillb DJ (2014) Development of a rapid, effective method for seeding biofiltration systems using alginate bead-immobilized cells. Int J Chem Environ Eng 5

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  CAS  Google Scholar 

  • Margesin R, Moertelmaier C, Mair J (2013) Low-temperature biodegradation of petroleum hydrocarbons (n-alkanes, phenol, anthracene, pyrene) by four actinobacterial strains. Int Biodeterior Biodegradation 84:185–191

    Article  CAS  Google Scholar 

  • Martin F et al (2012) Betaproteobacteria dominance and diversity shifts in the bacterial community of a PAH-contaminated soil exposed to phenanthrene. Environ Pollut 162:345–353

    Article  CAS  Google Scholar 

  • Mattes TE, Alexander AK, Richardson PM, Munk AC, Han CS, Stothard P, Coleman NV (2008) 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 74:6405–6416

    Article  CAS  Google Scholar 

  • Mosmeri H, Alaie E, Shavandi M, Dastgheib SMM, Tasharrofi S (2017a) Benzene-contaminated groundwater remediation using calcium peroxide nanoparticles: synthesis and process optimization. Environ Monit Assess 189:452

    Article  CAS  Google Scholar 

  • Mosmeri H, Alaie E, Shavandi M, Dastgheib SMM, Tasharrofi S (2017b) Bioremediation of benzene from groundwater by calcium peroxide (CaO2) nanoparticles encapsulated in sodium alginate. J Taiwan Inst Chem Eng 78:299–306

    Article  CAS  Google Scholar 

  • Mosmeri H, Gholami F, Shavandi M, Alaie E, Dastgheib SMM (2018a) Application of magnesium peroxide (MgO 2) nanoparticles for toluene remediation from groundwater: batch and column studies. Environ Sci Pollut Res:1–11

  • Mosmeri H, Tasharrofi S, Alaie E, Hassani SS (2018b) Controlled-release oxygen nanocomposite for bioremediation of benzene contaminated groundwater. In: New polymer nanocomposites for environmental remediation. Elsevier, pp 601–622

  • Mosmeri H, Gholami F, Shavandi M, Dastgheib SMM, Alaie E (2019) Bioremediation of benzene-contaminated groundwater by calcium peroxide (CaO2) nanoparticles: continuous-flow and biodiversity studies. J Hazard Mater 371:183–190

    Article  CAS  Google Scholar 

  • Muangchinda C, Rungsihiranrut A, Prombutara P, Soonglerdsongpha S, Pinyakong O (2018) 16S metagenomic analysis reveals adaptability of a mixed-PAH-degrading consortium isolated from crude oil-contaminated seawater to changing environmental conditions. J Hazard Mater 357:119–127. https://doi.org/10.1016/j.jhazmat.2018.05.062

    Article  CAS  Google Scholar 

  • Nestler H, Kiesel B, Kaschabek SR, Mau M, Schlömann M, Balcke GU (2007) Biodegradation of chlorobenzene under hypoxic and mixed hypoxic-denitrifying conditions. Biodegradation 18:755–767

    Article  CAS  Google Scholar 

  • Padula AM et al (2015) Ambient polycyclic aromatic hydrocarbons and pulmonary function in children. J Expo Sci Environ Epidemiol 25:295

    Article  CAS  Google Scholar 

  • Parales RE (2010) Hydrocarbon degradation by Betaproteobacteria. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 1715–1724. https://doi.org/10.1007/978-3-540-77587-4_121

    Chapter  Google Scholar 

  • Paulik LB, Hobbie KA, Rohlman D, Smith BW, Scott RP, Kincl L, Haynes EN, Anderson KA (2018) Environmental and individual PAH exposures near rural natural gas extraction. Environ Pollut 241:397–405

    Article  CAS  Google Scholar 

  • Prieto MB, Hidalgo A, Serra JL, Llama MAJ (2002) Degradation of phenol by Rhodococcus erythropolis UPV-1 immobilized on Biolite® in a packed-bed reactor. J Biotechnol 97:1–11

    Article  CAS  Google Scholar 

  • Schippers A, Bosecker K, Spröer C, Schumann P (2005) Microbacterium oleivorans sp. nov. and Microbacterium hydrocarbonoxydans sp. nov., novel crude-oil-degrading Gram-positive bacteria. Int J Syst Evol Microbiol 55:655–660

    Article  CAS  Google Scholar 

  • Schloss PD et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Shao Y et al (2015a) Biodegradation of PAHs by Acinetobacter isolated from karst groundwater in a coal-mining area. Environ Earth Sci 73:7479–7488. https://doi.org/10.1007/s12665-014-3920-3

    Article  CAS  Google Scholar 

  • Shao Z, Yuan J, Lai Q, Zheng T (2015b) The diversity of PAH-degrading bacteria in a deep-sea water column above the Southwest Indian Ridge. Front Microbiol 6:853

    Google Scholar 

  • Singh P, Singh VK, Singh R, Borthakur A, Kumar A, Tiwary D, Mishra PK (2018) Biological degradation of toluene by indigenous bacteria Acinetobacter junii CH005 isolated from petroleum contaminated sites in India. Energy Ecol Environ 3:162–170. https://doi.org/10.1007/s40974-018-0089-8

    Article  Google Scholar 

  • Sperfeld M, Rauschenbach C, Diekert G, Studenik S (2018) Microbial community of a gasworks aquifer and identification of nitrate-reducing Azoarcus and Georgfuchsia as key players in BTEX degradation. Water Res 132:146–157

    Article  CAS  Google Scholar 

  • Sun Y, Wang T, Peng X, Wang P, Lu Y (2016) Bacterial community compositions in sediment polluted by perfluoroalkyl acids (PFAAs) using Illumina high-throughput sequencing. Environ Sci Pollut Res 23:10556–10565

    Article  CAS  Google Scholar 

  • Táncsics A, Szabó I, Baka E, Szoboszlay S, Kukolya J, Kriszt B, Márialigeti K (2010) Investigation of catechol 2, 3-dioxygenase and 16S rRNA gene diversity in hypoxic, petroleum hydrocarbon contaminated groundwater. Syst Appl Microbiol 33:398–406

    Article  CAS  Google Scholar 

  • Unell M, Kabelitz N, Jansson JK, Heipieper HJ (2006) Adaptation of the psychrotroph Arthrobacter chlorophenolicus A6 to growth temperature and the presence of phenols by changes in the anteiso/iso ratio of branched fatty acids. FEMS Microbiol Lett 266:138–143

    Article  CAS  Google Scholar 

  • Unell M, Nordin K, Jernberg C, Stenström J, Jansson JK (2008) Degradation of mixtures of phenolic compounds by Arthrobacter chlorophenolicus A6. Biodegradation 19:495–505

    Article  CAS  Google Scholar 

  • Uz I, Duan Y, Ogram A (2000) Characterization of the naphthalene-degrading bacterium, Rhodococcus opacus M213. FEMS Microbiol Lett 185:231–238

    Article  CAS  Google Scholar 

  • Vila J, Tauler M, Grifoll M (2015) Bacterial PAH degradation in marine and terrestrial habitats. Curr Opin Biotechnol 33:95–102. https://doi.org/10.1016/j.copbio.2015.01.006

    Article  CAS  Google Scholar 

  • Wang D et al (2017) Biostimulation and microbial community profiling reveal insights on RDX transformation in groundwater. Microbiol Open 6:e00423

    Article  CAS  Google Scholar 

  • Westerberg K, Elväng AM, Stackebrandt E, Jansson JK (2000) Arthrobacter chlorophenolicus sp. nov., a new species capable of degrading high concentrations of 4-chlorophenol. Int J Syst Evol Microbiol 50:2083–2092

    Article  CAS  Google Scholar 

  • Wood WA, Krieg NR (1989) Methods for general and molecular bacteriology. Am Soc Microbiol

  • Xu X, Zhang Z, Hu S, Ruan Z, Jiang J, Chen C, Shen Z (2017) Response of soil bacterial communities to lead and zinc pollution revealed by Illumina MiSeq sequencing investigation. Environ Sci Pollut Res 24:666–675

    Article  CAS  Google Scholar 

  • Yan Y, Rene ER, Ma M, Ma W, Li X, Lun X (2018) Role of sulfate on the potential biodegradation of pentabromodiphenyl ether (BDE-99) in soil columns with reclaimed water and microbial community. Int Biodeterior Biodegradation 132:1–9

    Article  CAS  Google Scholar 

  • Yeh C-H, Lin C-W, Wu C-H (2010) A permeable reactive barrier for the bioremediation of BTEX-contaminated groundwater: microbial community distribution and removal efficiencies. J Hazard Mater 178:74–80

    Article  CAS  Google Scholar 

  • Yu S, Ke L, Wong Y, Tam N (2005) Degradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. Environ Int 31:149–154

    Article  CAS  Google Scholar 

  • Yuan H, Yao J, Masakorala K, Wang F, Cai M, Yu C (2014) Isolation and characterization of a newly isolated pyrene-degrading Acinetobacter strain USTB-X. Environ Sci Pollut Res 21:2724–2732. https://doi.org/10.1007/s11356-013-2221-9

    Article  CAS  Google Scholar 

  • Zhao D, Liu C, Liu L, Zhang Y, Liu Q, Wu W-M (2011) Selection of functional consortium for crude oil-contaminated soil remediation. Int Biodeterior Biodegradation 65:1244–1248

    Article  CAS  Google Scholar 

  • Zhao Q, Hu H, Wang W, Peng H, Zhang X (2015) Genome sequence of Sphingobium yanoikuyae B1, a polycyclic aromatic hydrocarbon-degrading strain. Genome Announc 3:e01522-01514

    Google Scholar 

  • Zhao Q, Yue S, Bilal M, Hu H, Wang W, Zhang X (2017) Comparative genomic analysis of 26 Sphingomonas and Sphingobium strains: dissemination of bioremediation capabilities, biodegradation potential and horizontal gene transfer. Sci Total Environ 609:1238–1247

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research has been supported by the National Iranian Oil Company (NIOC), Research and Technology Directorate under contract number 71/92019. The authors are grateful to Dr. Hosseinali Asgharian for reading and editing the English text. Our thanks and appreciation also go to the people who are directly or indirectly helped us out in developing this research.

Author information

Authors and Affiliations

  1. Extremophiles Laboratory, Department of Microbiology, College of Science, University of Tehran, Tehran, Iran

    Fatemeh Gholami & Mohammad Ali Amoozegar

  2. Ecology and Environmental Pollution Control Research Group, Research Institute of Petroleum Industry, P.O. Box: 14665-137, Tehran, Iran

    Mahmoud Shavandi

  3. Microbiology and Biotechnology Group, Research Institute of Petroleum Industry, Tehran, Iran

    Seyed Mohammad Mehdi Dastgheib

Authors
  1. Fatemeh Gholami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahmoud Shavandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seyed Mohammad Mehdi Dastgheib
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohammad Ali Amoozegar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mahmoud Shavandi.

Additional information

Responsible editor: Robert Duran

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 85 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gholami, F., Shavandi, M., Dastgheib, S.M.M. et al. The impact of calcium peroxide on groundwater bacterial diversity during naphthalene removal by permeable reactive barrier (PRB). Environ Sci Pollut Res 26, 35218–35226 (2019). https://doi.org/10.1007/s11356-019-06398-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06398-y

Keywords

Search

Navigation