Abstract
To bioaugment contaminated soil, the behavior of inoculated microorganisms in the soil must first be understood. In this study, Pseudomonas sp. DTF1, a diesel-degrading bacterium, was isolated from the rhizosphere of tall fescue (Festuca arundinacea) to investigate its diesel-degrading properties in aqueous and soil environments. In an aqueous environment, Pseudomonas sp. DTF1 degraded diesel at a rate of 7309–7882 mg L−1·d−1 for 10,000–30,000 mg diesel L−1. Pseudomonas sp. DTF1 efficiently degraded high-weight alkanes with 20–26 carbons in diesel, and the DTF1 strain could also utilize lubricant oil and pyrene. More specifically, this bacterium can produce biosurfactants, and its alkB gene was associated with the degradation of diesel. By inoculating Pseudomonas sp. DTF1 into diesel-contaminated soil, the diesel removal efficiency was increased from 15% (without inoculation) to 55% in 14 days. Although there was no significant difference in the 16S rRNA gene copy numbers, which represent bacterial abundance, the relative alkB gene copy numbers of the soil inoculated with the DTF1 strain were 4.7–9.5 times higher than those of the soil without inoculated microorganisms. Additionally, the relative abundance of Pseudomonas was over 60% in the soil inoculated with Pseudomonas sp. DTF1. The results suggest that Pseudomonas sp. DTF1 contributed significantly to diesel degradation during bioaugmentation by increasing the alkB gene abundance of the soil microorganism community.
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Abatenh E, Gizaw B, Tsegaye Z, Wassie M (2017) The role of microorganisms in bioremediation—A review. Open J Environ Biol 2:038–046. https://doi.org/10.17352/ojeb.000007
Adeline, Ting SY, Carol, Tan HC, Aw CS (2009) Hydrocarbon-degradation by isolate Pseudomonas Iundensis UTAR FPE2. Malays J Microbiol 5:104–108
Aisien FA, Chiadikobi JC, Aisien ET (2009) Toxicity assessment of some crude oil contaminated soils in the Niger delta. Open J Adv Mater Res 62:451–455. https://doi.org/10.4028/www.scientific.net/AMR.62-64.451
Aleer S, Adetutu EM, Makadia TH et al (2011) Harnessing the hydrocarbon-degrading potential of contaminated soils for the bioremediation of waste engine oil. Water Air Soil Pollut 218:121–130. https://doi.org/10.1007/s11270-010-0628-1
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. https://doi.org/10.1016/j.biortech.2004.09.008
Bharathi D, Rajalakshmi G, Komathi S (2019) Optimization and production of lipase enzyme from bacterial strains isolated from petrol spilled soil. J King Saud Univ Sci 31:898–901. https://doi.org/10.1016/j.jksus.2017.12.018
Bidja Abena MT, Chen G, Chen Z, Zheng X, Li S et al (2020) Microbial diversity changes and enrichment of potential petroleum hydrocarbon degraders in crude oil-, diesel-, and gasoline-contaminated soil. 3 Biotech 10(2):1–15
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in Solid sequencing. Nat Publ Gr 7:335–336. https://doi.org/10.1038/nmeth0510-335
Chicca I, Becarelli S, Dartiahl C et al (2020) Degradation of BTEX mixture by a new Pseudomonas putida strain: role of the quorum sensing in the modulation of the upper BTEX oxidative pathway. Environ Sci Pollut Res 27:36203–36214. https://doi.org/10.1007/s11356-020-09650-y
Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Environ Microbiol 53:224–229. https://doi.org/10.1128/aem.53.2.224-229.1987
Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol Res Int 2011:1–13. https://doi.org/10.4061/2011/941810
Fan Y, Wang J, Gao C et al (2020) A novel exopolysaccharide-producing and long-chain n-alkane degrading bacterium Bacillus licheniformis strain DM-1 with potential application for in-situ enhanced oil recovery. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-65432-z
Grace Liu PW, Chang TC, Whang LM et al (2011) Bioremediation of petroleum hydrocarbon contaminated soil: effects of strategies and microbial community shift. Int Biodeterior Biodegrad 65:1119–1127. https://doi.org/10.1016/j.ibiod.2011.09.002
Gran-Scheuch A, Fuentes E, Bravo DM et al (2017) Isolation and characterization of phenanthrene degrading bacteria from diesel fuel-contaminated Antarctic soils. Front Microbiol 8:1–12. https://doi.org/10.3389/fmicb.2017.01634
Hentati O, Lachhab R, Ayadi M, Ksibi M (2013) Toxicity assessment for petroleum-contaminated soil using terrestrial invertebrates and plant bioassays. Environ Monit Assess 185:2989–2998. https://doi.org/10.1007/s10661-012-2766-y
Herlemann DPR, Labrenz M, Jürgens K et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41
Hua F, Wang HQ, Li Y, Zhao YC (2013) Trans-membrane transport of n-octadecane by Pseudomonas sp. DG17. J Microbiol 51:791–799. https://doi.org/10.1007/s12275-013-3259-6
Hussain I, Puschenreiter M, Gerhard S et al (2018) Rhizoremediation of petroleum hydrocarbon-contaminated soils: improvement opportunities and field applications. Environ Exp Bot 147:202–219. https://doi.org/10.1016/j.envexpbot.2017.12.016
Ibrahim HMM (2016) Biodegradation of used engine oil by novel strains of Ochrobactrum anthropi HM-1 and Citrobacter freundii HM-2 isolated from oil-contaminated soil. 3 Biotech 6:1–13. https://doi.org/10.1007/s13205-016-0540-5
Imron MF, Kurniawan SB, Ismail N’I, Abdullah SRS (2020) Future challenges in diesel biodegradation by bacteria isolates: a review. J Clean Prod 251:119716. https://doi.org/10.1016/j.jclepro.2019.119716
Kaczorek E, Pacholak A, Zdarta A, Smułek W (2018) The impact of biosurfactants on microbial cell properties leading to hydrocarbon bioavailability increase. Colloids and Interfaces 2:35. https://doi.org/10.3390/colloids2030035
Kadnikov VV, Lomakina AV, Likhoshvai AV et al (2013) Composition of the microbial communities of bituminous constructions at natural oil seeps at the bottom of lake Baikal. Microbiol Russian Fed 82:373–382. https://doi.org/10.1134/S0026261713030168
Kalme S, Ghodake G, Govindwar S (2007) Red HE7B degradation using desulfonation by Pseudomonas desmolyticum NCIM 2112. Int Biodeterior Biodegrad 60:327–333. https://doi.org/10.1016/j.ibiod.2007.05.006
Kao CM, Chen CY, Chen SC et al (2008) Application of in situ biosparging to remediate a petroleum-hydrocarbon spill site: field and microbial evaluation. Chemosphere 70:1492–1499. https://doi.org/10.1016/j.chemosphere.2007.08.029
Kaur R, Mavi GK, Raghav S (2019) Bioremediation of sludge using Pseudomonas aeruginosa. Int J Curr Microbiol Appl Sci 8:69–79. https://doi.org/10.20546/ijcmas.2019.804.009
Kim TG, Lee EH, Cho KS (2011) Microbial community analysis of a methane-oxidizing biofilm using ribosomal tag pyrosequencing. J Microbiol Biotechnol 22:360–370. https://doi.org/10.4014/jmb.1109.09052
Kis ÁE, Laczi K, Zsíros S et al (2017) Characterization of the Rhodococcus sp. MK1 strain and its pilot application for bioremediation of diesel oil-contaminated soil. Acta Microbiol Immunol Hung 64:463–482. https://doi.org/10.1556/030.64.2017.037
Kohno T, Sugimoto Y, Sei K, Mori K (2002) Design of PCR primers and gene probes for general detection of alkane-degrading bacteria. Microbe Environ 17:114–121. https://doi.org/10.1264/jsme2.17.114
Kong W, Zhao C, Gao X et al (2021) Characterization and transcriptome analysis of a long-chain n-alkane-degrading strain Acinetobacter pittii sw-1. Int J Environ Res Public Health 18:1–15. https://doi.org/10.3390/ijerph18126365
Lee EH, Cho KS (2008) Characterization of cyclohexane and hexane degradation by Rhodococcus sp. EC1. Chemosphere 71:1738–1744. https://doi.org/10.1016/j.chemosphere.2007.12.009
Lee EH, Kim J, Cho KS et al (2010) Degradation of hexane and other recalcitrant hydrocarbons by a novel isolate, Rhodococcus sp. EH831. Environ Sci Pollut Res 17:64–77. https://doi.org/10.1007/s11356-009-0238-x
Lee SY, Kim SH, Lee DG et al (2014) Draft genome sequence of petroleum oil-degrading marine bacterium Pseudomonas taeanensis strain MS-3, isolated from a crude oil-contaminated seashore. Genome Announc 2:3–4. https://doi.org/10.1128/genomeA.e00818-13
Lee YY, Seo Y, Ha M et al (2021) Evaluation of rhizoremediation and methane emission in diesel-contaminated soil cultivated with tall fescue (Festuca arundinacea). Environ Res 194:110606. https://doi.org/10.1016/j.envres.2020.110606
Li W, Fu L, Niu B et al (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13:656–668. https://doi.org/10.1093/bib/bbs035
Li Q, Huang Y, Wen D et al (2020) Application of alkyl polyglycosides for enhanced bioremediation of petroleum hydrocarbon-contaminated soil using Sphingomonas changbaiensis and Pseudomonas stutzeri. Sci Total Environ 719:137456. https://doi.org/10.1016/j.scitotenv.2020.137456
Li X, Wu S, Dong Y et al (2021) Engineering microbial consortia towards bioremediation. Water (switzerland) 13:1–10. https://doi.org/10.3390/w13202928
Liao X, Luo J, Cassidy DP et al (2021) Biodegradation of phenanthrene at high concentrations by Acidovorax sp. JG5 and its functional genomic analysis. J Chem Technol Biotechnol 96:3142–3151. https://doi.org/10.1002/jctb.6867
Logeshwaran P, Megharaj M, Chadalavada S et al (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. https://doi.org/10.1016/j.eti.2018.02.001
Luo Q, Zhan JG, Shen XR et al (2013) Characterization of a novel diesel oil-degrading Pseudomonas sp. strain F4. Fresen Environ Bull 22:689–697
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Maia M, Capão A, Procópio L (2019) Biosurfactant produced by oil-degrading Pseudomonas putida AM-b1 strain with potential for microbial enhanced oil recovery. Bioremed J 23:302–310. https://doi.org/10.1080/10889868.2019.1669527
Mitri S, Clarke E, Foster KR (2016) Resource limitation drives spatial organization in microbial groups. ISME J 10:1471–1482. https://doi.org/10.1038/ismej.2015.208
Mrozik A, Piotrowska-Seget Z (2010) Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiol Res 165:363–375. https://doi.org/10.1016/j.micres.2009.08.001
Niazy Z, Hassanshahian M, Ataei A (2016) Isolation and characterization of diesel-degrading Pseudomonas strains from diesel-contaminated soils in Iran (Fars province). Pollution 2:67–75. https://doi.org/10.7508/pj.2016.01.00
Nwinyi OC, Olawore YA (2017) Biostimulation of spent engine oil contaminated soil using Ananas comosus and Solanum tuberosum peels. Environ Technol Innov 8:373–388. https://doi.org/10.1016/j.eti.2017.09.003
Obayori OS, Ilori MO, Adebusoye SA et al (2009) Degradation of hydrocarbons and biosurfactant production by Pseudomonas sp. strain LP1. World J Microbiol Biotechnol 25:1615–1623. https://doi.org/10.1007/s11274-009-0053-z
Österreicher-Cunha P, Vargas EDA, Guimarães JRD et al (2004) Evaluation of bioventing on a gasoline-ethanol contaminated undisturbed residual soil. J Hazard Mater 110:63–76. https://doi.org/10.1016/j.jhazmat.2004.02.037
Oualha M, Al-Kaabi N, Al-Ghouti M, Zouari N (2019) Identification and overcome of limitations of weathered oil hydrocarbons bioremediation by an adapted Bacillus sorensis strain. J Environ Manage 250:109455. https://doi.org/10.1016/j.jenvman.2019.109455
Pacwa-Płociniczak M, Czapla J, Płociniczak T, Piotrowska-Seget Z (2019) The effect of bioaugmentation of petroleum-contaminated soil with Rhodococcus erythropolis strains on removal of petroleum from soil. Ecotoxicol Environ Saf 169:615–622. https://doi.org/10.1016/j.ecoenv.2018.11.081
Paria S (2008) Surfactant-enhanced remediation of organic contaminated soil and water. Adv Colloid Interface Sci 138:24–58. https://doi.org/10.1016/j.cis.2007.11.001
Rahman KSM, Rahman TJ, McClean S et al (2002a) Rhamnolipid biosurfactant production by strains of Pseudomonas aeruginosa using low-cost raw materials. Biotechnol Prog 18:1277–1281. https://doi.org/10.1021/bp020071x
Rahman KSM, Thahira-Rahman J, Lakshmanaperumalsamy P, Banat IM (2002b) Towards efficient crude oil degradation by a mixed bacterial consortium. Bioresour Technol 85:257–261. https://doi.org/10.1016/S0960-8524(02)00119-0
Rajasekar A, Ting YP (2010) Microbial corrosion of aluminum 2024 aeronautical alloy by hydrocarbon degrading bacteria Bacillus cereus ACE4 and Serratia marcescens ACE2. Ind Eng Chem Res 49:6054–6061. https://doi.org/10.1021/ie100078u
Ramadass K, Megharaj M, Venkateswarlu K, Naidu R (2018) Bioavailability of weathered hydrocarbons in engine oil-contaminated soil: impact of bioaugmentation mediated by Pseudomonas spp. on bioremediation. Sci Total Environ 636:968–974. https://doi.org/10.1016/j.scitotenv.2018.04.379
Safdari MS, Kariminia HR, Ghobadi Nejad Z, Fletcher TH (2017) Study potential of indigenous Pseudomonas aeruginosa and Bacillus subtilis in bioremediation of diesel-contaminated water. Water Air Soil Poll 228:1–7. https://doi.org/10.1007/s11270-016-3220-5
Seo Y, Cho KS (2020) Rhizoremdiation of petroleum hydrocarbon-contaminated soils and greenhouse gas emission characteristics: a review. Microbiolo Biotechnol Lett 48:99–112. https://doi.org/10.4014/mbl.1911.11014
Singleton DR, Lee J, Dickey AN et al (2018) Polyphasic characterization of four soil-derived phenanthrene-degrading Acidovorax strains and proposal of Acidovorax carolinensis sp. nov. Syst Appl Microbiol 41:460–472. https://doi.org/10.1016/j.syapm.2018.06.001
Suja F, Rahim F, Taha MR et al (2014) Effects of local microbial bioaugmentation and biostimulation on the bioremediation of total petroleum hydrocarbons (TPH) in crude oil contaminated soil based on laboratory and field observations. Int Biodeterior Biodegrad 90:115–122. https://doi.org/10.1016/j.ibiod.2014.03.006
Vidonish JE, Zygourakis K, Masiello CA et al (2016) Thermal treatment of hydrocarbon-impacted soils: a review of technology innovation for sustainable remediation. Engineering 2:426–437. https://doi.org/10.1016/J.ENG.2016.04.005
Walter V, Syldatk C, Hausmann R (2010) Screening concepts for the isolation of biosurfactant producing microorganisms. Adv Exp Med Biol 672:1–13. https://doi.org/10.1007/978-1-4419-5979-9_1
Wang Z (2011) Bioavailability of organic compounds solubilized in nonionic surfactant micelles. Appl Microbiol Biotechnol 89:523–534. https://doi.org/10.1007/s00253-010-2938-z
Wang Y, Nie M, Wan Y et al (2017) Functional characterization of two alkane hydroxylases in a versatile Pseudomonas aeruginosa strain NY3. Ann Microbiol 67:459–468. https://doi.org/10.1007/s13213-017-1271-5
Wasmund K, Burns KA, Kurtböke DI, Bourne DG (2009) Novel alkane hydroxylase gene (alkB) diversity in sediments associated with hydrocarbon seeps in the Timor Sea, Australia. Appl Environ Microbiol 75:7391–7398. https://doi.org/10.1128/AEM.01370-09
Wongsa P, Tanaka M, Ueno A et al (2004) Isolation and characterization of novel strains of Pseudomonas aeruginosa and Serratia marcescens possessing high efficiency to degrade gasoline, kerosene, diesel oil, and lubricating oil. Curr Microbiol. https://doi.org/10.1007/s00284-004-4347-y
Wu T, Xu J, Xie W et al (2018) Pseudomonas aeruginosa L10: a hydrocarbon-degrading, biosurfactant-producing, and plant-growth-promoting endophytic bacterium isolated from a reed (Phragmites australis). Front Microbiol 9:1–12. https://doi.org/10.3389/fmicb.2018.01087
Wu T, Xu J, Liu J et al (2019) Characterization and initial application of endophytic Bacillus safensis strain ZY16 for improving phytoremediation of oil-contaminated saline soils. Front Microbiol 10:1–9. https://doi.org/10.3389/fmicb.2019.00991
Xia M, Liu Y, Taylor AA, Fu D, Khan AR et al (2017) Crude oil depletion by bacterial strains isolated from a petroleum hydrocarbon impacted solid waste management site in California. Int Biodeterior Biodegrad 123:70–77. https://doi.org/10.1016/j.ibiod.2017.06.003
Yang S, Wen X, Shi Y et al (2016) Hydrocarbon degraders establish at the costs of microbial richness, abundance and keystone taxa after crude oil contamination in permafrost environments. Sci Rep 6(1):1–13. https://doi.org/10.1038/srep37473
Yun MW, Jeong JH, Chang SW et al (2005) Biodegradation of diesel with Pseudomonas sp, KDi19 in liquid medium. J Korean Soc Environ Eng 27:1285–1291
Zhang Z, Hou Z, Yang C et al (2011) Degradation of n-alkanes and polycyclic aromatic hydrocarbons in petroleum by a newly isolated Pseudomonas aeruginosa DQ8. Bioresour Technol 102:4111–4116. https://doi.org/10.1016/j.biortech.2010.12.064
Zhang X, Bao D, Li M et al (2021a) Bioremediation of petroleum hydrocarbons by alkali–salt-tolerant microbial consortia and their community profiles. J Chem Technol Biotechnol 96:809–817. https://doi.org/10.1002/jctb.6594
Zhang X, Li R, Wang J et al (2021b) Construction of conductive network using magnetite to enhance microflora interaction and petroleum hydrocarbons removal in plant-rhizosphere microbial electrochemical system. Chem Eng J 433:133600. https://doi.org/10.1016/j.cej.2021.133600
Zhu H, Aitken MD (2010) Surfactant-enhanced desorption and biodegradation of polycyclic aromatic hydrocarbons in contaminated soil. Environ Sci Technol 44:7260–7265. https://doi.org/10.1021/es100112a
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This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean Government through the Ministry of Science and ICT (MSIT) (2019R1A2C2006701).
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Data curation, visualization, validation, writing-original draft and review were done by HY; data curation was done by GK; and review, edition, and supervision were done by K-SC.
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Yang, H., Kim, G. & Cho, KS. Bioaugmentation of diesel-contaminated soil with Pseudomonas sp. DTF1. Int. J. Environ. Sci. Technol. 20, 12499–12510 (2023). https://doi.org/10.1007/s13762-023-04846-4
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DOI: https://doi.org/10.1007/s13762-023-04846-4