Skip to main content
SpringerLink
Log in

Fungal proliferation and hydrocarbon removal during biostimulation of oily sludge with high total petroleum hydrocarbon

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

Abstract

A laboratory-scale study was conducted to investigate the effect of bioaugmentation (BA) and biostimulation (BS) on the remediation of oily sludge with high total petroleum hydrocarbon (TPH) content (269,000 mg/kg d.w. sludge). TPH concentration significantly decreased by 30.4% (P < 0.05) in the BS treatment after 13-week incubation, and 17.0 and 9.1% of TPH was removed in the BA and control treatments (amended with sterile water only), respectively. Aliphatic and other fractions (i.e., saturated n-alkanes and cyclic saturated alkanes) were reduced in the BS treatment, whereas no decrease in aromatic hydrocarbons occurred in any treatment. Gas chromatography–mass spectrometry analysis of aliphatic fractions showed that low-chain-length alkanes (C8–C20) were the most biodegradable fractions. The BS treatment supported fungal proliferation, with Sordariomycetes and Eurotiomycetes as the dominant classes. BS increased fungal diversity and decreased fungal abundance, and changed bacterial community structure. The findings show the potential of using BS to treat oily sludge with high TPH content.

Graphical abstract

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
Fig. 4

Similar content being viewed by others

References

  • Adetutu EM, Bird C, Kadali KK, Bueti A, Shahsavari E, Taha M, Patil S, Sheppard PJ, Makadia T, Simons KL, Ball AS (2015) Exploiting the intrinsic hydrocarbon-degrading microbial capacities in oil tank bottom sludge and waste soil for sludge bioremediation. Int J Environ Sci Technol 12:1427–1436

    Article  CAS  Google Scholar 

  • Al-Hawash AB, Zhang X, Ma F (2018) Removal and biodegradation of different petroleum hydrocarbons using the filamentous fungus Aspergillus sp. RFC-1. Microbiologyopen 619:1–14

    Google Scholar 

  • Al-Saleh E, Hassan A (2016) Enhanced crude oil biodegradation in soil via biostimulation. Int J Phytoremediation 18:822–831

    Article  CAS  Google Scholar 

  • April TM, Abbott SP, Foght JM, Currah RS (1998) Degradation of hydrocarbons in crude oil by the ascomycete Pseudallescheria boydii (Microascaceae). Can J Microbiol 44:270–278

    Article  CAS  Google Scholar 

  • Asgari A, Nabizadeh R, Mahvi AH, Nasseri S, Dehghani MH, Nazmara S, Yaghmaeian K (2017) Biodegradation of total petroleum hydrocarbons from acidic sludge produced by re-refinery industries of waste oil using in-vessel composting. J Environ Health Sci 15:3–11. https://doi.org/10.1186/s40201-017-0267-1

    Article  CAS  Google Scholar 

  • Ayotamuno JM, Kogbara RB, Taleat MO (2006) Bioremediation of a petroleum-hydrocarbon polluted agricultural soil at different levels of water application in Port Harcourt, Nigeria. J Food Agric Environ 4:214–217

    CAS  Google Scholar 

  • Bardi A, Yuan Q, Tigini V, Spina F, Varese GC, Spennati F, Becarelli S, Di Gregorio S, Petroni G, Munz G (2017) Recalcitrant compounds removal in raw leachate and synthetic effluents using the white-rot fungus Bjerkandera adusta. Water 9:824–837. https://doi.org/10.3390/w9110824

    Article  CAS  Google Scholar 

  • Becarelli S, Chicca I, Siracusa G, La China S, Gentini A, Lorenzi R, Munz G, Petroni G, Levin DB, Di Gregorio S (2019) Hydrocarbonoclastic Ascomycetes to enhance co-composting of total petroleum hydrocarbon (TPH) contaminated dredged sediments and lignocellulosic matrices. New Biotechnol 50:27–36

    Article  CAS  Google Scholar 

  • Bento FM, Camargo FAO, Okeke BC, Frankenberger WT (2005) Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresour Technol 96:1049–1055

    Article  CAS  Google Scholar 

  • Bovio E, Gnavi G, Prigione V, Spina F, Denaro R, Yakimov M, Calogero R, Crisafi F, Varese GC (2017) The culturable mycobiota of a Mediterranean marine site after an oil spill: isolation, identification and potential application in bioremediation. Sci Total Environ 576:310–318

    Article  CAS  Google Scholar 

  • Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Castiglione MR, Giorgetti L, Becarelli S, Siracusa G, Lorenzi R, Di Gregorio S (2016) Polycyclic aromatic hydrocarbon-contaminated soils: bioaugmentation of autochthonous bacteria and toxicological assessment of the bioremediation process by means of Vicia faba L. Environ Sci Pollut Res 23:1–12

    Article  Google Scholar 

  • Chen X, Luo S (2014) Analysis of Xinjiang coal, oil, natural gas production and consumption trend. Ecol Econ 42:1–57 (in Chinese)

    Google Scholar 

  • Di Gregorio S, Giorgetti L, Castiglione MR, Mariotti L, Lorenzi R (2015) Phytoremediation for improving the quality of effluents from a conventional tannery wastewater treatment plant. Int J Environ Sci Te 12:1387–1400

    Article  CAS  Google Scholar 

  • Di Gregorio S, Siracusa G, Becarelli S, Mariotti L, Gentini A, Lorenzi R (2016) Isolation and characterization of a hydrocarbonoclastic bacterial enrichment from total petroleum hydrocarbon contaminated sediments: potential candidates for bioaugmentation in bio-based processes. Environ Sci Pollut Res 23:10587–10594

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  Google Scholar 

  • Essabri AMA, Aydinlik NP, Williams NE (2019) Bioaugmentation and biostimulation of total petroleum hydrocarbon degradation in a petroleum-contaminated soil with fungi isolated from olive oil effluent. Water Air Soil Poll 230:76–91

    Article  CAS  Google Scholar 

  • Gurav R, Lyu H, Ma J, Tang J, Liu Q, Zhang H (2017) Degradation of n-alkanes and PAHs from the heavy crude oil using salt-tolerant bacterial consortia and analysis of their catabolic genes. Environ Sci Pollut Res 24:1–12

    Article  CAS  Google Scholar 

  • He Y, Duan X, Liu Y (2015) Enhanced bioremediation of oily sludge using co-culture of specific bacterial and yeast strains. J Chem Technol Biotechnol 89:1785–1792

    Article  CAS  Google Scholar 

  • Hu G, Li J, Zeng G (2013) Recent development in the treatment of oily sludge from petroleum industry: a review. J Hazard Mater 261:470–490

    Article  CAS  Google Scholar 

  • Huesemann MH, Hausmann TS, Fortman TJ (2002) Microbial factors father than bioavailability limit the rate and extent of PAH biodegradation in aged crude oil contaminated model soils. Bioremediat J 6:321–336

    Article  CAS  Google Scholar 

  • Ji C, Yang Y, Han W, He Y, Smith J, Smith P (2014) Climatic and edaphic controls on soil pH in alpine grasslands on the Tibetan Plateau, China: a quantitative analysis. Pedosphere 24:39–44

    Article  CAS  Google Scholar 

  • Joubert AVP, Lucas L, Garrido F, Joulian C, Jauzein M (2007) Effect of temperature, gas phase composition, pH and microbial activity on As, Zn, Pb and Cd mobility in selected soils in the Ebro and Meuse Basins in the context of global change. Environ Pollut 148:749–758

    Article  CAS  Google Scholar 

  • Lazar I, Dobrota S, Voicu A, Stefanescu M, Sandulescu L, Petrisor IG (1999) Microbial degradation of waste hydrocarbons in oily sludge from some Romanian oil fields. J Pet Sci Eng 22:151–160

    Article  CAS  Google Scholar 

  • Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315

    CAS  Google Scholar 

  • Liu PWG, Chang TC, Whang LM, Kao CH, Pan PT, Cheng SS (2011) Bioremediation of petroleum hydrocarbon contaminated soil: effects of strategies and microbial community shift. Int Biodeterior Biodegradation 65:1119–1127

    Article  CAS  Google Scholar 

  • Mansur AA, Taha M, Shahsavari E, Haleyur N, Adetutu EM, Ball AS (2016) An effective soil slurry bioremediation protocol for the treatment of Libyan soil contaminated with crude oil tank bottom sludge. Int Biodeterior Biodegradation 115:179–185

    Article  CAS  Google Scholar 

  • Meletiadis J, Meis JF, Mouton JW, Verweij PE (2001) Analysis of growth characteristics of filamentous fungi in different nutrient media. J Clin Microbiol 39:478–484

    Article  CAS  Google Scholar 

  • Mishra S, Jyot J, Kuhad RC, Lal B (2001) In situ bioremediation potential of an oily sludge-degrading bacterial consortium. Curr Microbiol 43:328–335. https://doi.org/10.1007/s002840010311

    Article  CAS  Google Scholar 

  • Morales LT, González-García LN, Orozco MC, Restrepo S, Vives MJ (2017) The genomic study of an environmental isolate of Scedosporium apiospermum shows its metabolic potential to degrade hydrocarbons. Stand Genomic Sci 12:71–82. https://doi.org/10.1186/s40793-017-0287-6

    Article  CAS  Google Scholar 

  • Patowary K, Patowary R, Kalita MC, Deka S (2016) Development of an efficient bacterial consortium for the potential remediation of hydrocarbons from contaminated sites. Front Microbiol 7:1–14

    Article  Google Scholar 

  • Payne RB, May HD, Sowers KR (2011) Enhanced reductive dechlorination of polychlorinated biphenyl impacted sediment by bioaugmentation with a dehalorespiring bacterium. Environ Sci Technol 45:8772–8779

    Article  CAS  Google Scholar 

  • Poi G, Aburto-Medina A, Mok PC, Ball AS, Shahsavari E (2017) Large scale bioaugmentation of soil contaminated with petroleum hydrocarbons using a mixed microbial consortium. Ecol Eng 102:64–71

    Article  Google Scholar 

  • Ramadass K, Smith E, Palanisami T, Mathieson G, Srivastava P, Megharaj M, Naidu R (2015) Evaluation of constraints in bioremediation of weathered hydrocarbon-contaminated arid soils through microcosm biopile study. Int J Environ Sci Technol 12:3597–3612

    Article  CAS  Google Scholar 

  • Reyes-César A, Absalón ÁE, Fernández FJ, González JM, Cortés-Espinosa DV (2014) Biodegradation of a mixture of PAHs by non-ligninolytic fungal strains isolated from crude oil-contaminated soil. World J Microbiol Biotechnol 30:999–1009

    Article  CAS  Google Scholar 

  • Rousk J, Frey SD (2016) Revisiting the hypothesis that fungal-to-bacterial dominance characterises turnover of soil organic matter and nutrients. Ecol Monogr 85:457–472

    Article  Google Scholar 

  • Roy A, Dutta A, Pal S, Gupta A, Sarkar J, Chatterjee A, Saha A, Sarkar P, Sar P, Kazy SK (2018) Biostimulation and bioaugmentation of native microbial community accelerated bioremediation of oil refinery sludge. Bioresour Technol 253:22–32

    Article  CAS  Google Scholar 

  • Sa Y (2009) Research and application on oily sludge treatment technology in Xinjiang oilfield. Environ Prot Oil Gas Fields 19:11–13 (in Chinese)

    Google Scholar 

  • Sarkar J, Kazy SK, Gupta A, Dutta A, Mohapatra B, Roy A, Bera P, Mitra A, Sar P (2016) Biostimulation of indigenous microbial community for bioremediation of petroleum refinery sludge. Front Microbiol 7:1–20

    Article  Google Scholar 

  • Schink B (2002) Synergistic interactions in the microbial world. Anton Leeuw 81:257–261. https://doi.org/10.1023/a:1020579004534

    Article  CAS  Google Scholar 

  • Schjønning P, Thomsen IK, Petersen SO, Kristensen K, Christensen BT (2011) Relating soil microbial activity to water content and tillage-induced differences in soil structure. Geoderma 163:256–264

    Article  CAS  Google Scholar 

  • Shuai Y, Zhou H, Mu Q, Zhang D, Zhang N, Tang J, Zhang C (2018) Characterization of a biosurfactant-producing Leclercia sp. B45 with new transcriptional patterns of alkB gene. Ann Microbiol 69:139–150

    Article  CAS  Google Scholar 

  • Simpanen S, Dahl M, Gerlach M, Mikkonen A, Malk V, Mikola J, Romantschuk M (2016) Biostimulation proved to be the most efficient method in the comparison of in situ soil remediation treatments after a simulated oil spill accident. Environ Sci Pollut Res 23:25024–25038

    Article  CAS  Google Scholar 

  • Siracusa G, Becarelli S, Lorenzi R, Gentini A, Di Gregorio S (2017) PCB in the environment: bio-based processes for soil decontamination and management of waste from the industrial production of Pleurotus ostreatus. New Biotechnol 39:232–239

    Article  CAS  Google Scholar 

  • Tyagi M, Fonseca MMR, Carvalho CCCR (2011) Bioaugmentation and biostimulation strategies to improve the effectiveness of bioremediation processes. Biodegradation 22:231–241

    Article  CAS  Google Scholar 

  • Vela S, Häggblom MM, Young LY (2002) Biodegradation of aromatic and aliphatic compounds by rhizobial species. Soil Sci 167:802–810

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  Google Scholar 

  • Wu M, Dick WA, Li W, Wang X, Yang Q, Wang T, Xu L, Zhang M, Chen L (2016) Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. Int Biodeterior Biodegradation 107:158–164

    Article  CAS  Google Scholar 

  • Wu M, Ye X, Chen K, Li W, Yuan J, Jiang X (2017) Bacterial community shift and hydrocarbon transformation during bioremediation of short-term petroleum-contaminated soil. Environ Pollut 223:657–664

    Article  CAS  Google Scholar 

  • Yanto DHY, Tachibana S (2014) Potential of fungal co-culturing for accelerated biodegradation of petroleum hydrocarbons in soil. J Hazard Mater 278:454–463

    Article  CAS  Google Scholar 

  • Ye C, Yang X, Zhao F, Ren L (2016) The shift of the microbial community in activated sludge with calcium treatment and its implication to sludge settleability. Bioresour Technol 207:11–18

    Article  CAS  Google Scholar 

  • Ying J, Brassington KJ, Prpich G, Paton GI, Semple KT, Pollard SJT, Coulon F (2016) Insights into the biodegradation of weathered hydrocarbons in contaminated soils by bioaugmentation and nutrient stimulation. Chemosphere 161:300–307

    Article  CAS  Google Scholar 

  • Yuan X, Zhang X, Chen X, Kong D, Liu X, Shen S (2018) Synergistic degradation of crude oil by indigenous bacterial consortium and exogenous fungus Scedosporium boydii. Bioresour Technol 264:190–197

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by XinJiang Keli New Technology Development Co., Ltd. (K17-529102-004), Karamay Major Science and Technology Project (2018ZD003B), and National Key Research and Development Program of China (2016YFE0123800).

Author information

Authors and Affiliations

  1. Institute of Marine Biology, Ocean College, Zhejiang University, Zhoushan, 316021, Zhejiang, China

    Hanghai Zhou, Xiaomin Huang, Dongdong Zhang & Chunfang Zhang

  2. Xinjiang Keli New Technology Development Co., Ltd., Karamay, 834000, Xinjiang, China

    Kuiyong Bu

  3. Xinjiang Academy of Environmental Protection Science, Urumqi, 830011, Xinjiang, China

    Fang Wen

Authors
  1. Hanghai Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaomin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kuiyong Bu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fang Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dongdong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chunfang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Dongdong Zhang or Chunfang Zhang.

Ethics declarations

Conflicts of interest

The authors declare that there is no conflict of interest.

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 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, H., Huang, X., Bu, K. et al. Fungal proliferation and hydrocarbon removal during biostimulation of oily sludge with high total petroleum hydrocarbon. Environ Sci Pollut Res 26, 33192–33201 (2019). https://doi.org/10.1007/s11356-019-06432-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06432-z

Keywords

Search

Navigation