Skip to main content
Log in

Bioremediation of petroleum-contaminated soils using Streptomyces sp. Hlh1

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Bioremediation using microorganisms is a promising strategy to remediate soil with petroleum hydrocarbons. Streptomyces sp. Hlh1, an endophytic strain, has previously demonstrated the ability to degrade crude petroleum in liquid culture. To apply this strain at field scale, it is necessary to test its ability to colonize the soil, compete with native microbiota, and remove the petroleum hydrocarbons under unfavorable conditions. Herein, a study was conducted to evaluate the performance of Streptomyces sp. Hlh1 to remove crude petroleum from contaminated sterilized and non-sterilized soils.

Materials and methods

Soils samples, contaminated with 2%, 5%, and 10% of petroleum, were inoculated with Streptomyces sp. Hlh1, and incubated at 30 °C for 4 weeks. At the end of bioremediation assays, the pollutant concentrations were determined by Gas chromatography flame ionization detector and the degradation rates were also calculated. The survival of the strain in the soil was estimated and the toxicity of metabolites was evaluated on Lactuca sativa.

Results and discussion

Streptomyces sp. Hlh1 was able to grow and remove total petroleum hydrocarbons (TPH), n-alkanes, and aromatic hydrocarbons found in soil samples. In sterilized soil samples, Streptomyces sp. Hlh1 removed up to 40% of TPH at an initial concentration of 10%. Whereas, the maximum TPH removal reached was 55% in non-sterilized soil at an initial concentration of 2%. In addition, it was observed that the degradation of aromatic hydrocarbons was more active than n-alkanes. The strain grew well and produced high biomass in contaminated soil. Lettuce seedling was found to be the adequate bioindicator to assess the toxicity of petroleum end products. Streptomyces sp. Hlh1 performed a successful bioremediation, which was confirmed through the phytotoxicity test.

Conclusions

The study shows the first insight of the contribution of free endophytic actinobacterial strain in the bioremediation of petroleum-contaminated soil; therefore, it suggests that Streptomyces sp. Hl1 can be usefully exploited at field scale.

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

Similar content being viewed by others

References

  • Abbasian F, Lockington R, Megharaj M, Naidu R (2016) The biodiversity changes in the microbial population of soils contaminated with crude oil. Curr Microbiol 72:663–670

    Article  CAS  Google Scholar 

  • Agnello AC, Bagard M, van Hullebusch ED, Esposito G, Huguenot D (2016) Comparative bioremediation of heavy metals and petroleum hydrocarbons co-contaminated soil by natural attenuation, phytoremediation, bioaugmentation and bioaugmentation-assisted phytoremediation. Sci Total Environ 563–564:693–703

    Article  CAS  Google Scholar 

  • Alvarez A, Saez JM, Davila Costa JS, Colin VL, Fuentes MS, Cuozzo SASA, Benimeli CS, Polti MA, Amoroso MJ (2017) Actinobacteria: current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere 166:41–62

    Article  CAS  Google Scholar 

  • Amoroso MJ, Benimeli CS, Cuozzo SA (2013) Actinobacteria: application in bioremediation and production of industrial enzymes. CRC Press, Boca Raton

  • Aparicio JD, Simón Solá MZ, Benimeli CS, Julia Amoroso M, Polti MA (2015) Versatility of Streptomyces sp. M7 to bioremediate soils co-contaminated with Cr (VI) and lindane. Ecotoxicol Environ Saf 116:34–39

    Article  CAS  Google Scholar 

  • Aparicio JD, Raimondo EE, Gil RA, Benimeli CS, Polti MA (2018) Actinobacteria consortium as an efficient biotechnological tool for mixed polluted soil reclamation: experimental factorial design for bioremediation process optimization. J Hazard Mater 342:408–417

    Article  CAS  Google Scholar 

  • Balachandran C, Duraipandiyan V, Balakrishna K, Ignacimuthu S (2012) Petroleum and polycyclic aromatic hydrocarbons (PAHs) degradation and naphthalene metabolism in Streptomyces sp. (ERI-CPDA-1) isolated from oil contaminated soil. Bioresour Technol 112:83–90

    Article  CAS  Google Scholar 

  • Bamgbose I, Anderson TA (2015) Phytotoxicity of three plant-based biodiesels, unmodified castor oil, and diesel fuel to alfalfa (Medicago sativa L.), lettuce (Lactuca sativa L.), radish (Raphanus sativus), and wheatgrass (Triticum aestivum). Ecotoxicol Environ Saf 122:268–274

    Article  CAS  Google Scholar 

  • Banks MK, Schultz KE (2005) Comparison of plants for germination toxicity tests in petroleum-contaminated soils. Water Air Soil Pollut 167:211–219

    Article  CAS  Google Scholar 

  • Baoune H, Ould El Hadj-Khelil A, Pucci G, Sineli P, Loucif L, Polti MA (2018) Petroleum degradation by endophytic Streptomyces spp. isolated from plants grown in contaminated soil of southern Algeria. Ecotoxicol Environ Saf 147:602–609

    Article  CAS  Google Scholar 

  • Barabás G, Vargha G, Szabó IM, Penyige A, Damjanovich S, Szöllösi J, Matkó J, Hirano T, Mátyus A, Szabó I (2001) n-Alkane uptake and utilisation by Streptomyces strains. Antonie Van Leeuwenhoek 79:269–276

    Article  Google Scholar 

  • Bidlan R, Afsar M, Manonmani HK (2004) Bioremediation of HCH-contaminated soil: elimination of inhibitory effects of the insecticide on radish and green gram seed germination. Chemosphere 56:803–811

    Article  CAS  Google Scholar 

  • Borah D, Yadav RNS (2017) Bioremediation of petroleum based contaminants with biosurfactant produced by a newly isolated petroleum oil degrading bacterial strain. Egypt J Pet 26:181–188

    Article  Google Scholar 

  • Bourguignon N, Bargiela R, Rojo D, Chernikova TN, de Rodas SAL, García-Cantalejo J, Näther DJ, Golyshin PN, Barbas C, Ferrero M, Ferrer M (2016) Insights into the degradation capacities of Amycolatopsis tucumanensis DSM 45259 guided by microarray data. World J Microbiol Biotechnol 32:201

    Article  CAS  Google Scholar 

  • Chen J, Zhang L, Jin Q, Su C, Zhao L, Liu X, Kou S, Wang Y, Xiao M (2017) Bioremediation of phenol in soil through using a mobile plant–endophyte system. Chemosphere 182:194–202

    Article  CAS  Google Scholar 

  • Das AJ, Kumar R (2016) Bioremediation of petroleum contaminated soil to combat toxicity on Withania somnifera through seed priming with biosurfactant producing plant growth promoting rhizobacteria. J Environ Manag 174:79–86

    Article  CAS  Google Scholar 

  • De Pasquale C, Palazzolo E, Lo PL, Quatrini P (2012) Degradation of long-chain n-alkanes in soil microcosms by two actinobacteria. J Environ Sci Health A 47:374–381

    Article  CAS  Google Scholar 

  • Fan M-Y, Xie R-J, Qin G (2014) Bioremediation of petroleum-contaminated soil by a combined system of biostimulation–bioaugmentation with yeast. Environ Technol 35:391–399

    Article  CAS  Google Scholar 

  • Franco JA, Bañón S, Vicente MJ, Miralles J, Martínez-Sánchez JJ (2011) Root development in horticultural plants grown under abiotic stress conditions - a review. J Hortic Sci Biotechnol 86:543–556

    Article  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 

  • Gargouri B, Karray F, Mhiri N, Aloui F, Sayadi S (2014) Bioremediation of petroleum hydrocarbons-contaminated soil by bacterial consortium isolated from an industrial wastewater treatment plant. J Chem Technol Biotechnol 89:978–987

    Article  CAS  Google Scholar 

  • Ghazali FM, Rahman RNZA, Salleh AB, Basri M (2004) Biodegradation of hydrocarbons in soil by microbial consortium. Int Biodeterior Biodegrad 54:61–67

    Article  CAS  Google Scholar 

  • Ghoreishi G, Alemzadeh A, Mojarrad M, Djavaheri M (2017) Bioremediation capability and characterization of bacteria isolated from petroleum contaminated soils in Iran. Sustain Environ Res 27:195–202

    Article  CAS  Google Scholar 

  • Guarino C, Spada V, Sciarrillo R (2017) Assessment of three approaches of bioremediation (natural attenuation, landfarming and bioagumentation – assistited landfarming) for a petroleum hydrocarbons contaminated soil. Chemosphere 170:10–16

    Article  CAS  Google Scholar 

  • Guo Q, Zhang J, Wan R, Xie S (2014) Impacts of carbon sources on simazine biodegradation by Arthrobacter strain SD3-25 in liquid culture and soil microcosm. Int Biodeterior Biodegrad 89:1–6

    Article  CAS  Google Scholar 

  • Huang L, Xie J, yi LB, Feng SX, Qiang LG, Lai LF, Yan LJ (2013) Optimization of nutrient component for diesel oil degradation by Acinetobacter beijerinckii ZRS. Mar Pollut Bull 76:325–332

    Article  CAS  Google Scholar 

  • Khan S, Afzal M, Iqbal S, Khan QM (2013) Plant–bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 90:1317–1332

    Article  CAS  Google Scholar 

  • Koshlaf E, Shahsavari E, Aburto-Medina A, Taha M, Haleyur N, Makadia TH, Morrison PD, Ball AS (2016) Bioremediation potential of diesel-contaminated Libyan soil. Ecotoxicol Environ Saf 133:297–305

    Article  CAS  Google Scholar 

  • Li X, Zhao L, Adam M (2016) Biodegradation of marine crude oil pollution using a salt-tolerant bacterial consortium isolated from Bohai Bay, China. Mar Pollut Bull 105:43–50

    Article  CAS  Google Scholar 

  • Liao J, Wang J, Jiang D, Wang MC, Huang Y (2015) Long-term oil contamination causes similar changes in microbial communities of two distinct soils. Appl Microbiol Biotechnol 99:10299–10310

    Article  CAS  Google Scholar 

  • Liu S-H, Zeng G-M, Niu Q-Y, Liu Y, Zhou L, Jiang L-H, Tan X, Xu P, Zhang C, Cheng M (2017) Bioremediation mechanisms of combined pollution of PAHs and heavy metals by bacteria and fungi: a mini review. Bioresour Technol 224:25–33

    Article  CAS  Google Scholar 

  • Logeshwaran P, Megharaj M, Chadalavada S, Bowman M, Naidu R (2018) Petroleum hydrocarbons (PH) in groundwater aquifers: an overview of environmental fate, toxicity, microbial degradation and risk-based remediation approaches. Environ Technol Innov 10:175–193

    Article  Google Scholar 

  • Luo Q, Hiessl S, Steinbüchel A (2014) Functional diversity of Nocardia in metabolism: metabolism of Nocardia. Environ Microbiol 16:29–48

    Article  CAS  Google Scholar 

  • Marchand C, St-Arnaud M, Hogland W, Bell TH, Hijri M (2017) Petroleum biodegradation capacity of bacteria and fungi isolated from petroleum-contaminated soil. Int Biodeterior Biodegrad 116:48–57

    Article  CAS  Google Scholar 

  • Margesin R, Hämmerle M, Tscherko D (2007) Microbial activity and community composition during bioremediation of diesel-oil-contaminated soil: effects of hydrocarbon concentration, fertilizers, and incubation time. Microb Ecol 53:259–269

    Article  CAS  Google Scholar 

  • Montagnolli RN, Lopes PRM, Bidoia ED (2015) Screening the toxicity and biodegradability of petroleum hydrocarbons by a rapid colorimetric method. Arch Environ Contam Toxicol 68:342–353

    Article  CAS  Google Scholar 

  • Pizzul L, del Pilar Castillo M, Stenström J (2006) Characterization of selected actinomycetes degrading polyaromatic hydrocarbons in liquid culture and spiked soil. World J Microbiol Biotechnol 22:745–752

    Article  CAS  Google Scholar 

  • Polti MA, Garcia RO, Amoroso MJ, Abate CM (2009) Bioremediation of chromium(VI) contaminated soil by Streptomyces sp. MC1. J Basic Microbiol 49:285–292

    Article  CAS  Google Scholar 

  • Polti MA, Atjian MC, Amoroso MJ, Abate CM (2011) Soil chromium bioremediation: synergic activity of actinobacteria and plants. Int Biodeterior Biodegrad 65:1175–1181

    Article  CAS  Google Scholar 

  • Polti MA, Aparicio JD, Benimeli CS, Amoroso MJ (2014) Simultaneous bioremediation of Cr(VI) and lindane in soil by actinobacteria. Int Biodeterior Biodegrad 88:48–55

    Article  CAS  Google Scholar 

  • Qin G, Gong D, Fan M-Y (2013) Bioremediation of petroleum-contaminated soil by biostimulation amended with biochar. Int Biodeterior Biodegrad 85:150–155

    Article  CAS  Google Scholar 

  • Roy AS, Baruah R, Borah M, Singh AK, Deka Boruah HP, Saikia N, Deka M, Dutta N, Chandra Bora T (2014) Bioremediation potential of native hydrocarbon degrading bacterial strains in crude oil contaminated soil under microcosm study. Int Biodeterior Biodegrad 94:79–89

    Article  CAS  Google Scholar 

  • Saez JM, Alvarez A, Benimeli CS, Amoroso MJ, Álvarez A, Benimeli CS, Amoroso MJ (2014) Enhanced lindane removal from soil slurry by immobilized Streptomyces consortium. Int Biodeterior Biodegrad 93:63–69

    Article  CAS  Google Scholar 

  • Saez JM, Bigliardo AL, Raimondo EE, Briceño G, Polti MA, Benimeli CS (2018) Lindane dissipation in a biomixture: effect of soil properties and bioaugmentation. Ecotoxicol Environ Saf 156:97–105

    Article  CAS  Google Scholar 

  • Sarkar D, Ferguson M, Datta R, Birnbaum S (2005) Bioremediation of petroleum hydrocarbons in contaminated soils: comparison of biosolids addition, carbon supplementation, and monitored natural attenuation. Environ Pollut 136:187–195

    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 

  • Seo J-S, Keum Y-S, Li QX (2012) Mycobacterium aromativorans JS19b1T degrades phenanthrene through C-1,2, C-3,4 and C-9,10 dioxygenation pathways. Int Biodeterior Biodegrad 70:96–103

    Article  CAS  Google Scholar 

  • Shahsavari E, Adetutu EM, Anderson PA, Ball AS (2013) Plant residues — a low cost, effective bioremediation treatment for petrogenic hydrocarbon-contaminated soil. Sci Total Environ 443:766–774

    Article  CAS  Google Scholar 

  • Shen F-T, Lin J-L, Huang C-C, Ho Y-N, Arun AB, Young L-S, Young C-C (2009) Molecular detection and phylogenetic analysis of the catechol 1,2-dioxygenase gene from Gordonia spp. Syst Appl Microbiol 32:291–300

    Article  CAS  Google Scholar 

  • U.S. EPA (1986) Test method for evaluating solid waste: Volume IC - Laboratory Manual, Physical/Chemical Methods (SW-846). United States Environmental Protection Agency, 3th edn. Washington, DC

  • Van Gestel K, Mergaert J, Swings J, Coosemans J, Ryckeboer J (2003) Bioremediation of diesel oil-contaminated soil by composting with biowaste. Environ Pollut 125:361–368

    Article  CAS  Google Scholar 

  • Varjani SJ (2017) Microbial degradation of petroleum hydrocarbons. Bioresour Technol 223:277–286

    Article  CAS  Google Scholar 

  • Wang B, Wang Q, Liu W, Liu X, Hou J, Teng Y, Luo Y, Christie P (2017) Biosurfactant-producing microorganism Pseudomonas sp. SB assists the phytoremediation of DDT-contaminated soil by two grass species. Chemosphere 182:137–142

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wu M, Li W, Dick WA, Ye X, Chen K, Kost D, Chen L (2017b) Bioremediation of hydrocarbon degradation in a petroleum-contaminated soil and microbial population and activity determination. Chemosphere 169:124–130

    Article  CAS  Google Scholar 

  • Zhao X, Liu W, Fu J, Cai Z, O’Reilly SE, Zhao D (2016) Dispersion, sorption and photodegradation of petroleum hydrocarbons in dispersant-seawater-sediment systems. Mar Pollut Bull 109:526–538

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge G. Borchia for his technical assistance and Enzo Raimondo for his invaluable contribution to this work.

Funding

This work was supported by “Secretaría de Ciencia, Arte e Innovación Tecnológica” of “Universidad Nacional de Tucumán” (PIUNT D504 and D626), “Agencia Nacional de Promoción Científica y Tecnológica” (PICT 2013 No. 0141; PICT 2016 No. 0493), and CONICET (PU-E 22920160100012CO).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marta Alejandra Polti.

Additional information

Responsible editor: Xilong Wang

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baoune, H., Aparicio, J.D., Pucci, G. et al. Bioremediation of petroleum-contaminated soils using Streptomyces sp. Hlh1. J Soils Sediments 19, 2222–2230 (2019). https://doi.org/10.1007/s11368-019-02259-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-019-02259-w

Keywords

Navigation