Abstract
A halotolerant bacterial strain was isolated from oily-contaminated sites of Persian Gulf, which characterized as Pseudomonas aeruginosa (AHV-KH10) by 16S rRNA gene sequencing. This strain was used for bioremediation of diesel-contaminated sediments. Biosurfactant production was initially screened by using oil displacement test and drop-collapse method, followed by measurement of surface tension (ST) of growth medium. Produced biosurfactant was a rhamnolipid type biosurfactant and lowered the ST to 33.4 mN/m at the given critical micelle concentration (CMC) of 75 mg/L. Addition of 3 CMC rhamnolipid, inoculums size of 15 mL, biodegradation in slurry phase and salinity level of 6% led totally to a diesel biodegradation rate of 70% for initial concentration of 1000 mg/kg after 35 days. The maximum diesel removal occurred at the salinity content of 6% indicating the moderately halo-tolerant characteristics of isolated strain. Evaluation of bacterial growth showed a biomass yield of 0.33 mg VSS/mg diesel in selected conditions. The field performance of Pseudomonas aeruginosa AHV-KH10 was proved through the removal of the TPH content in unwashed sediment, which varied from 2390 to 1875 mg/kg within four months.
Similar content being viewed by others
References
Agarwal A, Liu Y (2017) Enhanced microbubbles assisted cleaning of diesel contaminated sand. Marine Poll Bull 124:331–335. https://doi.org/10.1016/j.marpolbul.2017.07.041
Ahmadi M, Jorfi S, Kujlu R, Ghafari S, Soltani RDC, Haghighifard NJ (2017) A novel salt-tolerant bacterial consortium for biodegradation of saline and recalcitrant petrochemical wastewater. J Environ Manage 191:198–208. https://doi.org/10.1016/j.jenvman.2017.01.010
Alvim GM, Pontes PP (2018) Aeration and Sawdust Application Effects as Structural Material in the Bioremediation of Clayey Acid Soils Contaminated with Diesel Oil. I Int Soil Water Conser Res 6(3):253–260. https://doi.org/10.1016/j.iswcr.2018.04.002
Amin MM, Khiadani MH, Fatehizadeh A, Taheri E (2014) Validation of linear and non-linear kinetic modeling of saline wastewater treatment by sequencing batch reactor with adapted and non-adapted consortiums. Desalination 344:228–235. https://doi.org/10.1016/j.desal.2014.03.032
Avramova T, Sotirova A, Galabova D, Karpenko E (2008) Effect of Triton X-100 and rhamnolipid PS-17 on the mineralization of phenanthrene by Pseudomonas sp. cells. Int Biodeterior Biodegra 62:415–420. https://doi.org/10.1016/j.ibiod.2008.03.008
Ayed HB, Jemil N, Maalej H, Bayoudh A, Hmidet N, Nasri M (2015) Enhancement of solubilization and biodegradation of diesel oil by biosurfactant from Bacillus amyloliquefaciens An6. Int Biodeterior Biodegra 99:8–14. https://doi.org/10.1016/j.ibiod.2014.12.009
Bajagain R, Lee S, Jeong S-W (2018) Application of persulfate-oxidation foam spraying as a bioremediation pretreatment for diesel oil-contaminated soil. Chemosphere 207:565–572. https://doi.org/10.1016/j.chemosphere.2018.05.081
Bellagamba M, Cruz Viggi C, Ademollo N, Rossetti S, Aulenta F (2017) Electrolysis-driven bioremediation of crude oil-contaminated marine sediments. New Biotechnol 38:84–90. https://doi.org/10.1016/j.nbt.2016.03.003
Beolchini F, Ubaldini S, Passariello B, Gül N, Türe D, Vegliò F, Danovaro R, Dell’Anno A (2007) Bioremediation of dredged sediments polluted by heavy metals, Advanced Materials Research. Trans Tech Publ 20:307–310
Bernardez LA, Ghoshal S (2004) Selective solubilization of polycyclic aromatic hydrocarbons from multicomponent nonaqueous-phase liquids into nonionic surfactant micelles. Environ Sci Technol 38:5878–87. https://doi.org/10.1021/es0497429
Betancur-Corredor B, Pino NJ, Cardona S, Penuela GA (2015) Evaluation of biostimulation and Tween 80 addition for the bioremediation of long-term DDT-contaminated soil. J Environ Sci (China) 28:101–9. https://doi.org/10.1016/j.jes.2014.06.044
Bezza FA, Chirwa EMN (2017) The role of lipopeptide biosurfactant on microbial remediation of aged polycyclic aromatic hydrocarbons (PAHs)-contaminated soil. Chem Eng J 309:563–576. https://doi.org/10.1016/j.cej.2016.10.055
Chandankere R, Yao J, Choi MM, Masakorala K, Chan Y (2013) An efficient biosurfactant producing and crude-oil emulsifying bacterium Bacillus methylotrophicus USTBa isolated from petroleum reservoir. Biochem Eng J 74:46–53. https://doi.org/10.1016/j.bej.2013.02.018
Chang J-H, Qiang Z, Huang C-P, Ellis AV (2009) Phenanthrene removal in unsaturated soils treated by electrokinetics with different surfactants—Triton X-100 and rhamnolipid. Colloids and Surfaces Colloids Surf A Physicochem Eng Asp 348:157–163. https://doi.org/10.1016/j.colsurfa.2009.07.005
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2013) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucl Acids Res 42:D633–D642. https://doi.org/10.1093/nar/gkt1244
Cuypers C, Pancras T, Grotenhuis T, Rulkens W (2002) The estimation of PAH bioavailability in contaminated sediments using hydroxypropyl-beta-cyclodextrin and Triton X-100 extraction techniques. Chemosphere 46:1235–45. https://doi.org/10.1016/S0045-6535(01)00199-0
Dave BP, Ghevariya CM, Bhatt JK, Dudhagara DR, Rajpara RK (2014) Enhanced biodegradation of total polycyclic aromatic hydrocarbons (TPAHs) by marine halotolerant Achromobacter xylosoxidans using Triton X-100 and β-cyclodextrin – A microcosm approach. Marine Poll Bull 79:123–129. https://doi.org/10.1016/j.marpolbul.2013.12.027
Dell’Anno F, Sansone C, Ianora A, Dell’Anno A (2018) Biosurfactant-induced remediation of contaminated marine sediments: Current knowledge and future perspectives. Mar Environ Res 137:196–205. https://doi.org/10.1016/j.marenvres.2018.03.010
Fonti V, Beolchini F, Rocchetti L, Dell’Anno A (2015) Bioremediation of contaminated marine sediments can enhance metal mobility due to changes of bacterial diversity. Water Res 68:637–650. https://doi.org/10.1016/j.watres.2014.10.035
Freschi CR, Oliveira CJBd (2005) Comparison of DNA-extraction methods and selective enrichment broths on the detection of Salmonella Typhimurium in swine feces by polymerase chain reaction (PCR). Braz J Microbiol 36:363–367. https://doi.org/10.1590/S1517-83822005000400011
Garg M, Priyanka CM (2018) Isolation, characterization and antibacterial effect of biosurfactant from Candida parapsilosis. Biotechnol Rep (Amst). https://doi.org/10.1016/j.btre.2018.e00251
Ghojavand H, Vahabzadeh F, Roayaei E, Shahraki AK (2008) Production and properties of a biosurfactant obtained from a member of the Bacillus subtilis group (PTCC 1696). J Colloid Interface Sci 324:172–6. https://doi.org/10.1016/j.jcis.2008.05.001
Ghribi D, Abdelkefi-Mesrati L, Mnif I, Kammoun R, Ayadi I, Saadaoui I, Maktouf S, Chaabouni-Ellouze S (2012) Investigation of antimicrobial activity and statistical optimization of Bacillus subtilis SPB1 biosurfactant production in solid-state fermentation. J Biomed Biotechnol. https://doi.org/10.1155/2012/373682
Guerin TF (2015) Bioremediation of diesel from a rocky shoreline in an arid tropical climate. Marine Poll Bull 99:85–93. https://doi.org/10.1016/j.marpolbul.2015.07.059
Hajabbasi MA (2016) Importance of soil physical characteristics for petroleum hydrocarbons phytoremediation: A review. A Afr J Environ Sci Technol 10:394–405. https://doi.org/10.5897/AJEST2016.2169
Ibrahim ML, Ijah UJJ, Manga SB, Bilbis LS, Umar S (2013) Production and partial characterization of biosurfactant produced by crude oil degrading bacteria. Int Biodeterior Biodegrad 81:28–34. https://doi.org/10.1016/j.ibiod.2012.11.012
Ismail W, Alhamad N, El-Sayed W, El Nayal A, Chiang Y, Hamzah R (2013) Bacterial degradation of the saturate fraction of Arabian light crude oil: biosurfactant production and the effect of ZnO nanoparticles. J Pet Environ Biotechnol 4:163. https://doi.org/10.5454/mi.11.4.5
Jorfi S, Rezaee A, Mobeh-Ali G-A, Jaafarzadeh NA (2013) Application of biosurfactants produced by Pseudomonas aeruginosa SP4 for bioremediation of soils contaminated by pyrene. Soil and Sediment Contamination: An Int J 22:890–911. https://doi.org/10.1080/15320383.2013.770439
Jorfi S, Darvishi Cheshmeh Soltani R, Ahmadi M, Abtahi M, Ramavandi B, Zainab B (2017) Enhanced Sono-Fenton-Like Oxidation of PAHContaminated Soil Using Nano-Sized Magnetite as Catalyst: Optimization with Response Surface Methodology, Soil and Sediment Contamination. An Int J 26:538–557. https://doi.org/10.1080/15320383.2017.1363157
Joy S, Rahman PK, Sharma S (2017) Biosurfactant production and concomitant hydrocarbon degradation potentials of bacteria isolated from extreme and hydrocarbon contaminated environments. Chem Eng J 317:232–241. https://doi.org/10.1016/j.cej.2017.02.054
Kalantary RR, Mohseni-Bandpi A, Esrafili A, Nasseri S, Ashmagh FR, Jorfi S, Ja’fari M, (2014) Effectiveness of biostimulation through nutrient content on the bioremediation of phenanthrene contaminated soil. J Environ Health Sci Eng 12:143. https://doi.org/10.1186/s40201-014-0143-1
Karlapudi AP, Venkateswarulu T, Tammineedi J, Kanumuri L, Ravuru BK, ramu Dirisala V, Kodali VP, (2018) Role of biosurfactants in bioremediation of oil pollution-a review. Petroleum 4:241–249. https://doi.org/10.1016/j.petlm.2018.03.007
Kulik N, Goi A, Trapido M, Tuhkanen T (2006) Degradation of polycyclic aromatic hydrocarbons by combined chemical pre-oxidation and bioremediation in creosote contaminated soil. J Environ Manage 78:382–91. https://doi.org/10.1016/j.jenvman.2005.05.005
Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54(3):305–315
Lee DW, Lee H, Kwon BO, Khim JS, Yim UH, Kim BS, Kim JJ (2018) Biosurfactant-assisted bioremediation of crude oil by indigenous bacteria isolated from Taean beach sediment. Environ Pollut 241:254–264. https://doi.org/10.1016/j.envpol.2018.05.070
Mnif I, Sahnoun R, Ellouz-Chaabouni S, Ghribi D (2017) Application of bacterial biosurfactants for enhanced removal and biodegradation of diesel oil in soil using a newly isolated consortium. Process Process Saf Environ Protection 109:72–81. https://doi.org/10.1016/j.psep.2017.02.002
Moussa TAA, MM, N Samak, (2014) Production and characterization of di-rhamnolipid produced by Pseudomonas aeruginosa TMN. Braz J Chem Eng 31:867–880. https://doi.org/10.1590/0104-6632.20140314s00002473
Moya Ramirez I, Tsaousi K, Rudden M, Marchant R, Jurado Alameda E, Garcia Roman M, Banat IM (2015) Rhamnolipid and surfactin production from olive oil mill waste as sole carbon source. Bioresour Technol 198:231–6. https://doi.org/10.1016/j.biortech.2015.09.012
Mrozik AP-S, Labuzek S (2003) Bacterial Degradation and Bioremediation of Polycyclic Aromatic Hydrocarbons. Pol J Environ Stud. 12(1):15–25
Ni H, Zhou W, Zhu L (2014) Enhancing plant-microbe associated bioremediation of phenanthrene and pyrene contaminated soil by SDBS-Tween 80 mixed surfactants. J Environ Sci (China) 26:1071–1079. https://doi.org/10.1016/s1001-0742(13)60535-5
Patowary R, Patowary K, Kalita MC, Deka S (2018) Application of biosurfactant for enhancement of bioremediation process of crude oil contaminated soil. IInt Biodeterior Biodegrad 129:50–60. https://doi.org/10.1016/j.ibiod.2018.01.004
Pino-Herrera DO, Pechaud Y, Huguenot D, Esposito G, van Hullebusch ED, Oturan MA (2017) Removal mechanisms in aerobic slurry bioreactors for remediation of soils and sediments polluted with hydrophobic organic compounds: An overview. J Hazard Mater 339:427–449. https://doi.org/10.1016/j.jhazmat.2017.06.013
Pourfadakari S, Ahmadi M, Jaafarzadeh N, Takdastan A, Neisi AA, Ghafari S, Jorfi S (2019) Remediation of PAHs contaminated soil using a sequence of soil washing with biosurfactant produced by Pseudomonas aeruginosa strain PF2 and electrokinetic oxidation of desorbed solution, effect of electrode modification with Fe3O4 nanoparticles. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2019.120839
Pourfadakari S, Jorfi S, Ghafari S (2020) An Efficient Biosurfactant by Pseudomonas stutzeri Z12 Isolated from an Extreme Environment for Remediation of Soil Contaminated with Hydrocarbons. Chem Biochem Eng Quarter 34:35–48. https://doi.org/10.15255/CABEQ.2019.1718
Qin X, Tang J, Li D, Zhang Q (2012) Effect of salinity on the bioremediation of petroleum hydrocarbons in a saline-alkaline soil. Lett Appl Microbiol 55:210–217. https://doi.org/10.1111/j.1472-765X.2012.03280.x
Rikalović MG, Vrvić MM, Karadžić IM (2015) Rhamnolipid biosurfactant from Pseudomonas aeruginosa: from discovery to application in contemporary technology. J J Serb Chem Soc 80:279–304. https://doi.org/10.2298/JSC140627096R
Sharma PD (2005) Environmental Microbiology. Alpha Science International, Oxford
Singh P, Tiwary BN (2016) Isolation and characterization of glycolipid biosurfactant produced by a Pseudomonas otitidis strain isolated from Chirimiri coal mines. India Bioresour Bioprocess 3:42. https://doi.org/10.1186/s40643-016-0119-3
Subha B, Song YC, Woo JH (2017) Bioremediation of contaminated coastal sediment: Optimization of slow release biostimulant ball using response surface methodology (RSM) and stabilization of metals from contaminated sediment. Mar Pollut Bull 114:285–295. https://doi.org/10.1016/j.marpolbul.2016.09.034
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Varjani SJ, Upasani VN (2017) Critical review on biosurfactant analysis, purification and characterization using rhamnolipid as a model biosurfactant. Bioresour Technol 232:389–397. https://doi.org/10.1016/j.biortech.2017.02.047
Vaz DA, Gudina EJ, Alameda EJ, Teixeira JA, Rodrigues LR (2012) Performance of a biosurfactant produced by a Bacillus subtilis strain isolated from crude oil samples as compared to commercial chemical surfactants. Colloids Surf B Biointerfaces 89:167–74. https://doi.org/10.1016/j.colsurfb.2011.09.009
Vazquez S, Monien P, Pepino Minetti R, Jurgens J, Curtosi A, Villalba Primitz J, Frickenhaus S, Abele D, Mac Cormack W, Helmke E (2017) Bacterial communities and chemical parameters in soils and coastal sediments in response to diesel spills at Carlini Station, Antarctica. Sci Total Environ 605–606:26–37. https://doi.org/10.1016/j.scitotenv.2017.06.129
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991
Wu X, Du YG, Qu Y, Du DY (2013) Ternary cycle treatment of high saline wastewater from pesticide production using a salt-tolerant microorganism. Water Sci Technol 67:1960–6. https://doi.org/10.2166/wst.2013.072
Yang K, Zhu L, Xing B (2006) Enhanced soil washing of phenanthrene by mixed solutions of TX100 and SDBS. Environ Sci Technol 40:4274–4280. https://doi.org/10.1021/es060122c
Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J System Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Young JC, Clesceri LS, Kamhawy SM (2005) Changes in the biochemical oxygen demand procedure in the 21st edition of Standard Methods for the Examination of Water and Wastewater. Water Environ Res 77:404–410. https://doi.org/10.2175/106143005X51987
Zhang W (2015) Batch washing of saturated hydrocarbons and polycyclic aromatic hydrocarbons from crude oil contaminated soils using bio-surfactant. J Cent South Univ 22:895–903. https://doi.org/10.1007/s11771-015-2599-2
Zhao F, Zhou JD, Ma F, Shi RJ, Han SQ, Zhang J, Zhang Y (2016) Simultaneous inhibition of sulfate-reducing bacteria, removal of H2S and production of rhamnolipid by recombinant Pseudomonas stutzeri Rhl: Applications for microbial enhanced oil recovery. Bioresour Technol 207:24–30. https://doi.org/10.1016/j.biortech.2016.01.126
Acknowledgements
The funding of this study was provided by Ahvaz Jundishapur University of Medical Sciences (Grant no ETRC -9450).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pourfadakari, S., Ghafari, S., Takdastan, A. et al. A salt resistant biosurfactant produced by moderately halotolerant Pseudomonas aeruginosa (AHV-KH10) and its application for bioremediation of diesel-contaminated sediment in saline environment. Biodegradation 32, 327–341 (2021). https://doi.org/10.1007/s10532-021-09941-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-021-09941-2