Skip to main content
SpringerLink
Log in

Biodegradation of hydrocarbons by microbial strains in the presence of Ni and Pb

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Microbial strains capable of degrading petroleum hydrocarbons were isolated from the Yellow River Delta and screened for bio-surfactant production. The bio-surfactant-producing characteristics of the isolates were evaluated, and all the isolates which could produce bio-surfactant were identified by 16S rRNA gene sequencing. The results showed that the isolates belong to Bacillus sp. (72%), Ochrobactrum sp. (0.16%), Brevundimonas sp. (0.06%) and Brevibacterium sp. (0.06%). The biodegradability of crude oil, gasoline, diesel oil and other hydrocarbons by microbial strains were studied, among which the biodegrading ability of strain P1 and strain P19 is higher than other strains. Both strains P1 and P19 can degrade n-hexane and n-hexadecane effectively and have wide substrate extensiveness. In addition, Ni promoted the biodegradability of toluene by both strain P1 and strain P19, while Pb inhibited the growth of strain P19 and decreased its ability to biodegrade toluene. The studies revealed that microbes including strain P1 and strain P19 can be utilized in bioremediation of co-contaminated water with petroleum and heavy metals including Ni and Pb.

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
Fig. 5

Similar content being viewed by others

References

  • Abou-Shanab RA, Eraky M, Haddad AM, Abdel-Gaffar AB, Salem AM (2016) Characterization of crude oil degrading bacteria isolated from contaminated soils surrounding gas stations. Bull Environ Contam Toxicol 97:684–688

    Article  CAS  PubMed  Google Scholar 

  • Amani H, Muller MM, Syldatk C, Hausmann R (2013) Production of microbial rhamnolipid by Pseudomonas aeruginosa MM1011 for ex situ enhanced oil recovery. Appl Biochem Biotechnol 170:1080–1093

    Article  CAS  PubMed  Google Scholar 

  • Ayangbenro AS, Babalola OO (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 14:94

    Article  PubMed Central  CAS  Google Scholar 

  • Bai L, Luo Y, Shi D, Xie X, Li L, Zhou Y, Yan Z, Li F (2015) TOPSIS-based screening method of soil remediation technology for contaminated sites and its application. Soil Sediment Contam Int J 24:386–397

    Article  CAS  Google Scholar 

  • Batista SB, Mounteer AH, Amorim FR, Totola MR (2006) Isolation and characterization of biosurfactant/bioemulsifier-producing bacteria from petroleum contaminated sites. Bioresour Technol 97:868–875

    Article  CAS  PubMed  Google Scholar 

  • Bieszkiewicz E, Boszczyk-Maleszak H, Wlodarczyk A, Horoch M (2002) Studies on the effect of inoculation of activated sludge with bacteria actively degrading hydrocarbons on the biodegradation of petroleum products. Acta Microbiol Pol 51:285–292

    CAS  PubMed  Google Scholar 

  • Bodour AA, Miller-Maier RM (1998) Application of a modified drop-collapse technique for surfactant quantitation and screening of biosurfactant-producing microorganisms. J Microbiol Methods 32:273–280

    Article  CAS  Google Scholar 

  • Borah D, Yadav RNS (2014) Biodegradation of diesel, crude oil, kerosene and used engine oil by a newly isolated Bacillus cereus strain DRDU1 from an automobile engine in liquid culture. Arab J Sci Eng 39:5337–5345

    Article  CAS  Google Scholar 

  • Chen Q, Li J, Liu M, Sun H, Bao M (2017) Study on the biodegradation of crude oil by free and immobilized bacterial consortium in marine environment. PLoS ONE 12:e0174445

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cooper DG, Goldenberg BG (1987) Surface-active agents from two bacillus species. Appl Environ Microbiol 53:224–229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das P, Yang XP, Ma LZ (2014) Analysis of biosurfactants from industrially viable Pseudomonas strain isolated from crude oil suggests how rhamnolipids congeners affect emulsification property and antimicrobial activity. Front Microbiol 5:696

    PubMed  PubMed Central  Google Scholar 

  • Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Federici E, Giubilei M, Santi G, Zanaroli G, Negroni A, Fava F, Petruccioli M, D'Annibale A (2012) Bioaugmentation of a historically contaminated soil by polychlorinated biphenyls with Lentinus tigrinus. Microb Cell Fact 11:35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao L, Kano N, Sato Y, Li C, Zhang S, Imaizumi H (2012) Behavior and distribution of heavy metals including rare earth elements, thorium, and uranium in sludge from industry water treatment plant and recovery method of metals by biosurfactants application. Bioinorg Chem Appl 2012:173819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • George S, Jayachandran K (2013) Production and characterization of rhamnolipid biosurfactant from waste frying coconut oil using a novel Pseudomonas aeruginosa D. J Appl Microbiol 114:373–383

    Article  CAS  PubMed  Google Scholar 

  • Georgiou G, Lin SC, Sharma MM (1992) Surface-active compounds from microorganisms. Biotechnology (N Y) 10:60–65

    CAS  Google Scholar 

  • Goswami L, Arul Manikandan N, Pakshirajan K, Pugazhenthi G (2017) Simultaneous heavy metal removal and anthracene biodegradation by the oleaginous bacteria Rhodococcus opacus. Biotech 7:37

    Google Scholar 

  • Hausinger RP (1987) Nickel utilization by microorganisms. Microbiol Rev 51:22–42

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hazen TC et al (2010) Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330:204–208

    Article  CAS  PubMed  Google Scholar 

  • Iqbal A, Arshad M, Karthikeyan R, Gentry TJ, Rashid J, Ahmed I, Schwab AP (2019) Diesel degrading bacterial endophytes with plant growth promoting potential isolated from a petroleum storage facility. Biotech 9:35

    Google Scholar 

  • Irorere VU, Tripathi L, Marchant R, McClean S, Banat IM (2017) Microbial rhamnolipid production: a critical re-evaluation of published data and suggested future publication criteria. Appl Microbiol Biotechnol 101:3941–3951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jamal MT, Pugazhendi A (2018) Degradation of petroleum hydrocarbons and treatment of refinery wastewater under saline condition by a halophilic bacterial consortium enriched from marine environment (Red Sea), Jeddah. Saudi Arabia. Biotech 8:276

    Google Scholar 

  • Kaczorek E, Olszanowski A (2011) Uptake of hydrocarbon by Pseudomonas fluorescens (P1) and Pseudomonas putida (K1) strains in the presence of surfactants: a cell surface modification. Water Air Soil Pollut 214:451–459

    Article  CAS  PubMed  Google Scholar 

  • Kim DJ, Park MR, Lim DS, Choi JW (2013) Impact of nitrate dose on toluene degradation under denitrifying condition. Appl Biochem Biotechnol 170:248–256

    Article  CAS  PubMed  Google Scholar 

  • Klimek B, Sitarz A, Choczynski M, Niklinska M (2016) The effects of heavy metals and total petroleum hydrocarbons on soil bacterial activity and functional diversity in the Upper Silesia Industrial Region (Poland). Water Air Soil Pollut 227:265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Y, Guan Y, Gao B, Yue Q (2012) Antioxidant responses and degradation of two antibiotic contaminants in Microcystis aeruginosa. Ecotoxicol Environ Saf 86:23–30

    Article  CAS  PubMed  Google Scholar 

  • Lotfabad TB, Shourian M, Roostaazad R, Najafabadi AR, Adelzadeh MR, Noghabi KA (2009) An efficient biosurfactant-producing bacterium Pseudomonas aeruginosa MR01, isolated from oil excavation areas in south of Iran. Colloids Surf B Biointerfaces 69:183–193

    Article  CAS  PubMed  Google Scholar 

  • Luz AP, Pellizari VH, Whyte LG, Greer CW (2004) A survey of indigenous microbial hydrocarbon degradation genes in soils from Antarctica and Brazil. Can J Microbiol 50:323–333

    Article  CAS  PubMed  Google Scholar 

  • Maddela NR, Scalvenzi L, Venkateswarlu K (2017) Microbial degradation of total petroleum hydrocarbons in crude oil: a field-scale study at the low-land rainforest of Ecuador. Environ Technol 38:2543–2550

    Article  CAS  PubMed  Google Scholar 

  • Margesin R, Gander S, Zacke G, Gounot AM, Schinner F (2003) Hydrocarbon degradation and enzyme activities of cold-adapted bacteria and yeasts. Extremophiles 7:451–458

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Wefers P, Schmidt M, Knittel K, Kruger M, Stagars MH, Treude T (2017) Hydrocarbon degradation in Caspian Sea sediment cores subjected to simulated petroleum seepage in a newly designed sediment-oil-flow-through system. Front Microbiol 8:763

    Article  PubMed  PubMed Central  Google Scholar 

  • Mouton J, Mercier G, Drogui P, Blais JF (2009) Experimental assessment of an innovative process for simultaneous PAHs and Pb removal from polluted soils. Sci Total Environ 407:5402–5410

    Article  CAS  PubMed  Google Scholar 

  • Munguia T, Smith CA (2001) Surface tension determination through capillary rise and laser diffraction patterns. J Chem Educ 78:343

    Article  CAS  Google Scholar 

  • Nitschke M, Pastore GM (2006) Production and properties of a surfactant obtained from Bacillus subtilis grown on cassava wastewater. Bioresour Technol 97:336–341

    Article  CAS  PubMed  Google Scholar 

  • Noordman WH, Janssen DB (2002) Rhamnolipid stimulates uptake of hydrophobic compounds by Pseudomonas aeruginosa. Appl Environ Microbiol 68:4502–4508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okolo V, Olowolafe E, Okoduwa IA (2016) Effects of industrial effluents on soil resources in Challawa Industrial Area, Kano. Nigeria. Global J Environ Sci Manag 5(1):10

    Google Scholar 

  • Pacwa-Plociniczak M, Plaza GA, Poliwoda A, Piotrowska-Seget Z (2014) Characterization of hydrocarbon-degrading and biosurfactant-producing Pseudomonas sp. P-1 strain as a potential tool for bioremediation of petroleum-contaminated soil. Environ Sci Pollut Res Int 21:9385–9395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plociniczak T, Kukla M, Watroba R, Piotrowska-Seget Z (2013) The effect of soil bioaugmentation with strains of Pseudomonas on Cd, Zn and Cu uptake by Sinapis alba L. Chemosphere 91:1332–1337

    Article  CAS  PubMed  Google Scholar 

  • Qi YB, Wang CY, Lv CY, Lun ZM, Zheng CG (2017) Removal capacities of polycyclic aromatic hydrocarbons (PAHs) by a newly isolated strain from oilfield produced water. Int J Environ Res Public Health 14:215

    Article  PubMed Central  CAS  Google Scholar 

  • Qiu XH, Bai WQ, Zhong QZ, Li M, He FQ, Li BT (2006) Isolation and characterization of a bacterial strain of the genus Ochrobactrum with methyl parathion mineralizing activity. J Appl Microbiol 101:986–994

    Article  CAS  PubMed  Google Scholar 

  • Sachdev DP, Cameotra SS (2013) Biosurfactants in agriculture. Appl Microbiol Biotechnol 97:1005–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos DK, Rufino RD, Luna JM, Santos VA, Sarubbo LA (2016) Biosurfactants: multifunctional biomolecules of the 21st century. Int J Mol Sci 17:401

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma SL, Pant A (2000) Biodegradation and conversion of alkanes and crude oil by a marine Rhodococcus sp. Biodegradation 11:289–294

    Article  CAS  PubMed  Google Scholar 

  • Silkina A, Nelson GD, Bayliss CE, Pooley CL, Day JG (2017) Bioremediation efficacy-comparison of nutrient removal from an anaerobic digest waste-based medium by an algal consortium before and after cryopreservation. J Appl Phycol 29:1331–1341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sriram MI, Gayathiri S, Gnanaselvi U, Jenifer PS, Mohan Raj S, Gurunathan S (2011) Novel lipopeptide biosurfactant produced by hydrocarbon degrading and heavy metal tolerant bacterium Escherichia fergusonii KLU01 as a potential tool for bioremediation. Bioresour Technol 102:9291–9295

    Article  CAS  PubMed  Google Scholar 

  • Swati GP, Das MT, Thakur IS (2014) In vitro toxicity evaluation of organic extract of landfill soil and its detoxification by indigenous pyrene-degrading Bacillus sp. ISTPY1. Int Biodeterior Biodegradation 90:145–151

    Article  CAS  Google Scholar 

  • Valenzuela-Reyes E, Casas-Flores S, Isordia-Jasso I, Arriaga S (2014) Performance and bacterial population composition of an n-hexane degrading biofilter working under fluctuating conditions. Appl Biochem Biotechnol 174:832–844

    Article  CAS  PubMed  Google Scholar 

  • Viramontes-Ramos S, Cristina Portillo-Ruiz M, Ballinas-Casarrubias Mde L, Torres-Munoz JV, Rivera-Chavira BE, Nevarez-Moorillon GV (2010) Selection of biosurfactant/bioemulsifier-producing bacteria from hydrocarbon-contaminated soil. Braz J Microbiol 41:668–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Chen M, Xiao J, Hao L, Crowley DE, Zhang Z, Yu J, Huang N, Huo M, Wu J (2015) Genome sequence analysis of the naphthenic acid degrading and metal resistant bacterium Cupriavidus gilardii CR3. PLoS ONE 10:e0132881

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu SJ, Zhang LL, Wang JD, Chen JM (2007) Bacillus circulans WZ-12—a newly discovered aerobic dichloromethane-degrading methylotrophic bacterium. Appl Microbiol Biotechnol 76:1289–1296

    Article  CAS  PubMed  Google Scholar 

  • Xi J, Saingam P, Gu F, Hu HY, Zhao X (2014) Effect of continuous ozone injection on performance and biomass accumulation of biofilters treating gaseous toluene. Appl Microbiol Biotechnol 98:9437–9446

    Article  CAS  PubMed  Google Scholar 

  • Xia W, Du Z, Cui Q, Dong H, Wang F, He P, Tang Y (2014) Biosurfactant produced by novel Pseudomonas sp. WJ6 with biodegradation of n-alkanes and polycyclic aromatic hydrocarbons. J Hazard Mater 276:489–498

    Article  CAS  PubMed  Google Scholar 

  • Yadav BK, Shrestha SR, Hassanizadeh SM (2012) Biodegradation of toluene under seasonal and diurnal fluctuations of soil–water temperature. Water Air Soil Pollut 223:3579–3588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshikawa M, Zhang M, Toyota K (2017) Integrated anaerobic–aerobic biodegradation of multiple contaminants including chlorinated ethylenes, benzene, toluene, and dichloromethane. Water Air Soil Pollut 228:25

    Article  PubMed  CAS  Google Scholar 

  • Yousafzai AM, Ullah F, Bari F, Raziq S, Riaz M, Khan K, Nishan U, Sthanadar IA, Shaheen B, Shaheen M, Ahmad H (2017) Bioaccumulation of some heavy metals: analysis and comparison of Cyprinus carpio and Labeo rohita from Sardaryab Khyber Pakhtunkhwa. BioMed Res Int 2017:5801432

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Youssef NH, Duncan KE, Nagle DP, Savage KN, Knapp RM, McInerney MJ (2004) Comparison of methods to detect biosurfactant production by diverse microorganisms. J Microbiol Methods 56:339–347

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Yao H, Lu Y, Yu X, Wang J, Sun S, Liu M, Li D, Li YF, Zhang D (2017) Uptake and translocation of polycyclic aromatic hydrocarbons (PAHs) and heavy metals by maize from soil irrigated with wastewater. Sci Rep 7:12165

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang W, Liu YG, Tan XF, Zeng GM, Gong JL, Lai C, Niu QY, Tang YQ (2019) Enhancement of detoxification of petroleum hydrocarbons and heavy metals in oil-contaminated soil by using glycine-beta-cyclodextrin. Int J Environ Res Public Health 16:1155

    Article  CAS  PubMed Central  Google Scholar 

  • Zhong Q, Zhang H, Bai W, Li M, Li B, Qiu X (2007) Degradation of aromatic compounds and degradative pathway of 4-nitrocatechol by Ochrobactrum sp. B2. J Environ Sci Health A Tox Hazard Subst Environ Eng 42:2111–2116

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by National Natural Science Foundation of China (Project no. 31500094), Shandong Provincial Natural Science Foundation, China (Projection no. ZR2015EM018) as well as the Housing and Urban Construction Science and Technology Program (Grant no. 2017-K2-005).

Author information

Authors and Affiliations

  1. School of Municipal and Environmental Engineering, Shandong Jianzhu University, Jinan, 250101, China

    Chuanqing Zhong, Jia Zhao, Wenbing Chen & Daoji Wu

  2. Shandong Medicinal Biotechnology Center, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, 250062, China

    Guangxiang Cao

Authors
  1. Chuanqing Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jia Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenbing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daoji Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guangxiang Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guangxiang Cao.

Ethics declarations

Conflict of interest

The authors of this work declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhong, C., Zhao, J., Chen, W. et al. Biodegradation of hydrocarbons by microbial strains in the presence of Ni and Pb. 3 Biotech 10, 18 (2020). https://doi.org/10.1007/s13205-019-2011-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-019-2011-2

Keywords

Search

Navigation