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Journal of Soils and Sediments

, Volume 19, Issue 5, pp 2222–2230 | Cite as

Bioremediation of petroleum-contaminated soils using Streptomyces sp. Hlh1

  • Hafida Baoune
  • Juan Daniel Aparicio
  • Graciela Pucci
  • Aminata Ould El Hadj-Khelil
  • Marta Alejandra PoltiEmail author
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article

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.

Keywords

Bacteria Bioremediation Detoxification Persistent organic pollutants (POPs) Polycyclic aromatic hydrocarbons (PAHs) 

Notes

Acknowledgements

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

Funding information

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).

References

  1. Abbasian F, Lockington R, Megharaj M, Naidu R (2016) The biodiversity changes in the microbial population of soils contaminated with crude oil. Curr Microbiol 72:663–670CrossRefGoogle Scholar
  2. 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 563–564:693–703CrossRefGoogle Scholar
  3. 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 166:41–62CrossRefGoogle Scholar
  4. Amoroso MJ, Benimeli CS, Cuozzo SA (2013) Actinobacteria: application in bioremediation and production of industrial enzymes. CRC Press, Boca RatonGoogle Scholar
  5. 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 116:34–39CrossRefGoogle Scholar
  6. 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 342:408–417CrossRefGoogle Scholar
  7. 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 112:83–90CrossRefGoogle Scholar
  8. 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 122:268–274CrossRefGoogle Scholar
  9. Banks MK, Schultz KE (2005) Comparison of plants for germination toxicity tests in petroleum-contaminated soils. Water Air Soil Pollut 167:211–219CrossRefGoogle Scholar
  10. 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 147:602–609CrossRefGoogle Scholar
  11. 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 79:269–276CrossRefGoogle Scholar
  12. 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 56:803–811CrossRefGoogle Scholar
  13. 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 26:181–188CrossRefGoogle Scholar
  14. 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 32:201CrossRefGoogle Scholar
  15. 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 182:194–202CrossRefGoogle Scholar
  16. 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 174:79–86CrossRefGoogle Scholar
  17. 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 47:374–381CrossRefGoogle Scholar
  18. 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 35:391–399CrossRefGoogle Scholar
  19. 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 86:543–556CrossRefGoogle Scholar
  20. Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98:4781–4794CrossRefGoogle Scholar
  21. 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 89:978–987CrossRefGoogle Scholar
  22. Ghazali FM, Rahman RNZA, Salleh AB, Basri M (2004) Biodegradation of hydrocarbons in soil by microbial consortium. Int Biodeterior Biodegrad 54:61–67CrossRefGoogle Scholar
  23. 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 27:195–202CrossRefGoogle Scholar
  24. 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 170:10–16CrossRefGoogle Scholar
  25. 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 89:1–6CrossRefGoogle Scholar
  26. 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 76:325–332CrossRefGoogle Scholar
  27. Khan S, Afzal M, Iqbal S, Khan QM (2013) Plant–bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 90:1317–1332CrossRefGoogle Scholar
  28. 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 133:297–305CrossRefGoogle Scholar
  29. 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 105:43–50CrossRefGoogle Scholar
  30. 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 99:10299–10310CrossRefGoogle Scholar
  31. 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 224:25–33CrossRefGoogle Scholar
  32. 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 10:175–193CrossRefGoogle Scholar
  33. Luo Q, Hiessl S, Steinbüchel A (2014) Functional diversity of Nocardia in metabolism: metabolism of Nocardia. Environ Microbiol 16:29–48CrossRefGoogle Scholar
  34. 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 116:48–57CrossRefGoogle Scholar
  35. 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 53:259–269CrossRefGoogle Scholar
  36. Montagnolli RN, Lopes PRM, Bidoia ED (2015) Screening the toxicity and biodegradability of petroleum hydrocarbons by a rapid colorimetric method. Arch Environ Contam Toxicol 68:342–353CrossRefGoogle Scholar
  37. 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 22:745–752CrossRefGoogle Scholar
  38. Polti MA, Garcia RO, Amoroso MJ, Abate CM (2009) Bioremediation of chromium(VI) contaminated soil by Streptomyces sp. MC1. J Basic Microbiol 49:285–292CrossRefGoogle Scholar
  39. Polti MA, Atjian MC, Amoroso MJ, Abate CM (2011) Soil chromium bioremediation: synergic activity of actinobacteria and plants. Int Biodeterior Biodegrad 65:1175–1181CrossRefGoogle Scholar
  40. Polti MA, Aparicio JD, Benimeli CS, Amoroso MJ (2014) Simultaneous bioremediation of Cr(VI) and lindane in soil by actinobacteria. Int Biodeterior Biodegrad 88:48–55CrossRefGoogle Scholar
  41. Qin G, Gong D, Fan M-Y (2013) Bioremediation of petroleum-contaminated soil by biostimulation amended with biochar. Int Biodeterior Biodegrad 85:150–155CrossRefGoogle Scholar
  42. 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 94:79–89CrossRefGoogle Scholar
  43. 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 93:63–69CrossRefGoogle Scholar
  44. 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 156:97–105CrossRefGoogle Scholar
  45. 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 136:187–195CrossRefGoogle Scholar
  46. 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 163:256–264CrossRefGoogle Scholar
  47. 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 70:96–103CrossRefGoogle Scholar
  48. 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 443:766–774CrossRefGoogle Scholar
  49. 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 32:291–300CrossRefGoogle Scholar
  50. 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, DCGoogle Scholar
  51. Van Gestel K, Mergaert J, Swings J, Coosemans J, Ryckeboer J (2003) Bioremediation of diesel oil-contaminated soil by composting with biowaste. Environ Pollut 125:361–368CrossRefGoogle Scholar
  52. Varjani SJ (2017) Microbial degradation of petroleum hydrocarbons. Bioresour Technol 223:277–286CrossRefGoogle Scholar
  53. 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 182:137–142CrossRefGoogle Scholar
  54. 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 223:657–664CrossRefGoogle Scholar
  55. 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 169:124–130CrossRefGoogle Scholar
  56. 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 109:526–538CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Planta Piloto de Procesos Industriales Microbiológicos (PROIMI)CONICETTucumánArgentina
  2. 2.Laboratoire de protection des écosystème en zones arides et semi-arides, FNSVUniversité Kasdi Merbah OuraglaOuraglaAlgeria
  3. 3.Facultad de Bioquímica, Química y FarmaciaUniversidad Nacional de Tucumán (UNT)TucumánArgentina
  4. 4.Centro de Estudios e Investigación en Microbiología Aplicada (CEIMA)Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB)Comodoro RivadaviaArgentina
  5. 5.Facultad de Ciencias Naturales e Instituto Miguel LilloUniversidad Nacional de Tucumán (UNT)TucumánArgentina

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