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3 Biotech

, 10:42 | Cite as

Microbial diversity changes and enrichment of potential petroleum hydrocarbon degraders in crude oil-, diesel-, and gasoline-contaminated soil

  • Marie Thérèse Bidja Abena
  • Guoqing Chen
  • Zeyu Chen
  • Xiucheng Zheng
  • Shanshan Li
  • Tongtong Li
  • Weihong ZhongEmail author
Original Article
  • 26 Downloads

Abstract

This study investigated the impacts of crude oil, diesel, and gasoline on the diversity of indigenous microbial communities as well as culturable microorganisms in the studied soil. Oil contamination led to shifts in the diversity of the soil’s microbial communities, regardless of the contaminant applied. Unpolluted soils were more diverse and evenly distributed than contaminated samples. The domain Bacteria accounted for 65.15% of the whole microbial community. The bacterial phylum Proteobacteria dominated in all samples, followed by Actinobacteria and Acidobacteria. Pseudomonas with 28.15% of reads dominated in Proteobacteria, while Rhodococcus (3.07%) dominated in Actinobacteria, and Blastocatella (2.53%) dominated in Acidobacteria. The dominant fungal phyla across all samples were Ascomycota dominated by Penicillium (50.48% of sequences), and Zygomycota dominated by Mortierella (16.87%). Sequences similar to the archaeal phyla, Euryarchaeota and Thaumarchaeota, were also detected. The number of culturable microorganisms increased following the contamination and was higher in contaminated samples than in clean samples. Oil contamination also resulted in the enrichment of oil-degrading strains. Two bacteria, Serratia marcescens strain PL and Raoultella ornithinolytica PS, which were isolated from crude oil-contaminated soil, exhibited strong crude oil degradation ability. Strain PL was the most efficient strain and degraded 75.10% of crude oil, while strain PL degraded 65.48%, after 20 days of incubation. However, the mixed culture of the two strains was more effective than single strain and could achieve up to 96.83% of crude oil degradation, with a complete abatement of straight-chain hydrocarbons (from C12 to C25), and more than 91% removal of highly branched hydrocarbons, phytane and pristane, which are known to be more recalcitrant to biodegradation. Strains PS and PL are two newly isolated crude oil degraders that are not among the most prominent crude oil-degrading strains referenced in the literature. Therefore, their high degradation capacity makes them perfect candidates for the bioremediation of petroleum hydrocarbon contaminated environments.

Keywords

Raoultella ornithinolytica Diversity Microbial communities Crude oil Biodegradation 

Notes

Acknowledgements

This research was supported by the College of Biotechnology and Bioengineering at the Zhejiang University of Technology.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

13205_2019_2027_MOESM1_ESM.docx (457 kb)
Supplementary file1 (DOCX 456 kb)
13205_2019_2027_MOESM2_ESM.pdf (669 kb)
Supplementary file2 (PDF 668 kb)
13205_2019_2027_MOESM3_ESM.pdf (127 kb)
Supplementary file3 (PDF 126 kb)
13205_2019_2027_MOESM4_ESM.docx (21 kb)
Supplementary file4 (DOCX 20 kb)

References

  1. Agbor RB, Antai SP, Nkanang AJ (2018) Microbial degradation of total petroleum hydrocarbon in crude oil polluted soil ameliorated with agro-wastes. Glo J Earth Environ Sci 3:1–7CrossRefGoogle Scholar
  2. Albuquerque L, França L, Rainey FA et al (2011) Gaiella occulta gen. nov., sp. nov., a novel representative of a deep branching phylogenetic lineage within the class Actinobacteria and proposal of Gaiellaceae fam. nov. and Gaiellales ord. nov. Syst Appl Microbiol 34:595–599.  https://doi.org/10.1016/j.syapm.2011.07.001 CrossRefPubMedGoogle Scholar
  3. Alegbeleye OO, Opeolu BO, Jackson V (2017) Bioremediation of polycyclic aromatic hydrocarbon (PAH) compounds: (acenaphthene and fluorene) in water using indigenous bacterial species isolated from the Diep and Plankenburg rivers, Western Cape, South Africa. Braz J Microbiol 48:314–325.  https://doi.org/10.1016/j.bjm.2016.07.027 CrossRefPubMedGoogle Scholar
  4. Ameen F, Moslem M, Hadi S et al (2016) Biodegradation of diesel fuel hydrocarbons by mangrove fungi from Red Sea Coast of Saudi Arabia Saudi. J Biol Sci 23:211–218.  https://doi.org/10.1016/j.sjbs.2015.04.005 CrossRefGoogle Scholar
  5. Avanzi I, Gracioso L, Baltazar M et al (2015) Aerobic Biodegradation of Gasoline Compounds by Bacteria Isolated from a Hydrocarbon-Contaminated Soil. Environ Eng Sci 32:990–997.  https://doi.org/10.1089/ees.2015.0122 CrossRefGoogle Scholar
  6. Bidja Abena MT, Li T, Shah MN, Zhong W (2019) Biodegradation of total petroleum hydrocarbons (TPH) in highly contaminated soils by natural attenuation and bioaugmentation. Chemosphere 234:864–874.  https://doi.org/10.1016/j.chemosphere.2019.06.111 CrossRefPubMedGoogle Scholar
  7. Borowik A, Wyszkowska J, Oszust K (2017) Functional diversity of fungal communities in soil contaminated with diesel oil. Front Microbiol 8:1862.  https://doi.org/10.3389/fmicb.2017.01862 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen Q, Li J, Liu M et al (2017a) Study on the biodegradation of crude oil by free and immobilized bacterial consortium in marine environment. PLoS ONE 12(3):e0174445.  https://doi.org/10.1371/journal.pone.0174445 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen W, Li J, Sun X et al (2017b) High efficiency degradation of alkanes and crude oil by a salt-tolerant bacterium Dietzia species CN-3. Int Biodeter Biodegr 118:110–118CrossRefGoogle Scholar
  10. Crisafi F, Genovese M, Smedile F, Russo D, Catalfamo M, Yakimov M, Giuliano L, Denaro R (2016) Bioremediation technologies for polluted seawater sampled after an oil-spill in Taranto Gulf (Italy): a comparison of biostimulation, bioaugmentation and use of a washing agent in microcosm studies. Mar Pollut Bull 106:119–126CrossRefGoogle Scholar
  11. Das K, Mukherjee AK (2007) Crude petroleum-oil biodegradation efficiency of Bacillus subtilis and Pseudomonas aeruginosa strains isolated from a petroleum-oil contaminated soil from North-East India. Bioresource Technol 98:1339–1345.  https://doi.org/10.1016/j.biortech.2006.05.032 CrossRefGoogle Scholar
  12. Govarthanan M, Fuzisawa S, Hosogai T et al (2017) Biodegradation of aliphatic and aromatic hydrocarbons using the filamentous fungus Penicillium sp. CHY-2 and characterization of its manganese peroxidase activity. RSC Adv 7:20716–20723.  https://doi.org/10.1039/C6RA28687A CrossRefGoogle Scholar
  13. Hare JM (2013) Sabouraud agar for fungal growth. In: Gupta V, Tuohy M, Ayyachamy M (eds) Laboratory protocols in fungal biology. Springer, New YorkGoogle Scholar
  14. Hassanshahian M, Emtiazi G, Cappello S (2012) Isolation and characterization of crude-oil-degrading bacteria from the Persian Gulf and the Caspian Sea. Mar Pollut Bull 64:7–12.  https://doi.org/10.1016/j.marpolbul.2011.11.006 CrossRefPubMedGoogle Scholar
  15. Hazen TC, Prince RC, Mahmoudi N (2016) Marine oil biodegradation. Environ Sci Technol 50:2121–2129.  https://doi.org/10.1021/acs.est.5b03333 CrossRefPubMedGoogle Scholar
  16. Hughes KA, Bridge P, Clark MS (2007) Tolerance of antarctic soil fungi to hydrocarbons. Sci Total Environ 372:539–548.  https://doi.org/10.1016/j.scitotenv.2006.09.016 CrossRefPubMedGoogle Scholar
  17. Kirk JL, Beaudette LA, Hart M et al (2004) Methods of studying soil microbial diversity. J Microbiol Meth 58:169–188.  https://doi.org/10.1016/j.mimet.2004.04.006 CrossRefGoogle Scholar
  18. Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549.  https://doi.org/10.1093/molbev/msy096 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Lauber CL, Hamady M, Knight R et al (2009) Pyrosequencing-based assessment of soil ph as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111.  https://doi.org/10.1128/AEM.00335-09 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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
  21. Liu H, He H, Cheng C et al (2015) Diversity analysis of the bacterial community in tobacco waste extract during reconstituted tobacco process. Appl Microbiol Biotechnol 99(1):469–476.  https://doi.org/10.1007/s00253-014-5960-8 CrossRefPubMedGoogle Scholar
  22. Lu S-j, Wang H-q, Yao Z-h (2006) Isolation and characterization of gasoline-degrading bacteria from gas station leaking-contaminated soils. J Environ Sci 18:969–972.  https://doi.org/10.1016/S1001-0742(06)60023-5 CrossRefGoogle Scholar
  23. Ma L-N, Guo C-y, Lü X-T et al (2015) Soil moisture and land use are major determinants of soil microbial community composition and biomass at a regional scale in northeastern China. Biogeosciences 12:2585–2596.  https://doi.org/10.5194/bg-12-2585-2015 CrossRefGoogle Scholar
  24. Mahjoubi M, Cappello S, Souissi Y et al (2017) Microbial bioremediation of petroleum hydrocarbon—contaminated marine environments. In: Zoveidavianpoor M (ed) Recent insights in petroleum science and engineering. IntechOpen, LondonGoogle Scholar
  25. Morales-Guzmán G, Ferrera-Cerrato R, Rivera-Cruz MDC et al (2017) Diesel degradation by emulsifying bacteria isolated from soils polluted with weathered petroleum hydrocarbons. Appl Soil Ecol 121:127–134.  https://doi.org/10.1016/j.apsoil.2017.10.003 CrossRefGoogle Scholar
  26. Mrozik A, Piotrowska-Seget Z (2010) Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiol Res 165:363–375CrossRefGoogle Scholar
  27. Obi LU, Atagana HI, Adeleke RA (2016) Isolation and characterisation of crude oil sludge degrading bacteria. SpringerPlus 5:1946–1946.  https://doi.org/10.1186/s40064-016-3617-z CrossRefPubMedPubMedCentralGoogle Scholar
  28. Patowary K, Patowary R, Kalita MC, Deka S (2016) Development of an efficient bacterial consortium for the potential remediation of hydrocarbons from contaminated sites. Front Microbiol 7:1092.  https://doi.org/10.3389/fmicb.2016.01092 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Rahman KS, Thahira-Rahman J, Lakshmanaperumalsamy P et al (2002) Towards efficient crude oil degradation by a mixed bacterial consortium. Bioresource Technol 85:257–261CrossRefGoogle Scholar
  30. Rousk J, Bååth E, Brookes PC et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. Isme J 4:1340.  https://doi.org/10.1038/ismej.2010.58 CrossRefPubMedGoogle Scholar
  31. Roy AS, Baruah R, Borah M et al (2014) Bioremediation potential of native hydrocarbon degrading bacterial strains in crude oil contaminated soil under microcosm study. Int Biodeter Biodegr 94:79–89.  https://doi.org/10.1016/j.ibiod.2014.03.024 CrossRefGoogle Scholar
  32. Salam LB, Ilori MO, Amund OO et al (2018) Characterization of bacterial community structure in a hydrocarbon-contaminated tropical African soil. Environ Technol 39:939–951.  https://doi.org/10.1080/09593330.2017.1317838 CrossRefPubMedGoogle Scholar
  33. Santisi S, Cappello S, Catalfamo M et al (2015) Biodegradation of crude oil by individual bacterial strains and a mixed bacterial consortium. Braz J Microbiol 46:377–387.  https://doi.org/10.1590/s1517-838246120131276 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Sathishkumar M, Binupriya AR, Baik S-H et al (2008) Biodegradation of crude oil by individual bacterial strains and a mixed bacterial consortium isolated from hydrocarbon contaminated areas. Clean: Soil, Air, Water Air Water 36:92–96.  https://doi.org/10.1002/clen.200700042 CrossRefGoogle Scholar
  35. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864.  https://doi.org/10.1093/bioinformatics/btr026 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Siles JA, Margesin R (2018) Insights into microbial communities mediating the bioremediation of hydrocarbon-contaminated soil from an Alpine former military site. Appl Microbiol Biotechnol 102:4409–4421.  https://doi.org/10.1007/s00253-018-8932-6 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Stoica C, Sorescu I (2017) The great bacteria Book-ABIS online encyclopedia. Regnum Prokaryotae. https://tgw1916.net/ABIS/encyclopedia.html. Accessed on Mar 2017
  38. Sutton NB, Maphosa F, Morillo JA et al (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79:619–630.  https://doi.org/10.1128/aem.02747-12 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035.  https://doi.org/10.1073/pnas.0404206101 CrossRefPubMedGoogle Scholar
  40. Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol R 67:503–549.  https://doi.org/10.1128/MMBR.67.4.503-549.2003 CrossRefGoogle Scholar
  41. Varjania SJ, Rana DP, Jain AK et al (2015) Synergistic ex-situ biodegradation of crude oil by halotolerant bacterial consortium of indigenous strains isolated from on shore sites of Gujarat, India. Int Biodeter Biodegr 103:116–124CrossRefGoogle Scholar
  42. Waigi MG, Kang F, Goikavi C et al (2015) Phenanthrene biodegradation by sphingomonads and its application in the contaminated soils and sediments: a review. Int Biodeter Biodegr 104:333–349.  https://doi.org/10.1016/j.ibiod.2015.06.008 CrossRefGoogle Scholar
  43. Wilsey B, Stirling G (2007) Species richness and evenness respond in a different manner to propagule density in developing prairie microcosm communities. Plant Ecol 190:259–273.  https://doi.org/10.1007/s11258-006-9206-4 CrossRefGoogle Scholar
  44. Wu M, Ye X, Chen K et al (2017) Bacterial community shift and hydrocarbon transformation during bioremediation of short-term petroleum-contaminated soil. Environ Pollut 223:657–664.  https://doi.org/10.1016/j.envpol.2017.01.079 CrossRefPubMedGoogle Scholar
  45. Xia M, Liu Y, Taylor AA et al (2017) Crude oil depletion by bacterial strains isolated from a petroleum hydrocarbon impacted solid waste management site in California. Int Biodeter Biodegr 123:70–77.  https://doi.org/10.1016/j.ibiod.2017.06.003 CrossRefGoogle Scholar
  46. Yan S, Wang Q, Qu L et al (2013) Characterization of oil-degrading bacteria from oil-contaminated soil and activity of their enzymes. Biotechnol Biotec Eq 27:3932–3938.  https://doi.org/10.5504/BBEQ.2013.0050 CrossRefGoogle Scholar
  47. Yang S, Wen X, Jin H et al (2012) Pyrosequencing investigation into the bacterial community in permafrost soils along the China–Russia Crude Oil Pipeline (CRCOP). PLoS ONE 7:e52730.  https://doi.org/10.1371/journal.pone.0052730 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Yang R, Zhang G, Li S et al (2019) Degradation of crude oil by mixed cultures of bacteria isolated from the Qinghai–Tibet plateau and comparative analysis of metabolic mechanisms. Environ Sci Pollut Res 26(2):1834–1847.  https://doi.org/10.1007/s11356-018-3718-z CrossRefGoogle Scholar
  49. Zhao D, Liu C, Liu L et al (2011) Selection of functional consortium for crude oil-contaminated soil remediation. Int Biodeter Biodegr 65:1244–1248CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2020

Authors and Affiliations

  1. 1.College of Biotechnology and BioengineeringZhejiang University of TechnologyHangzhouChina
  2. 2.International CollegeZhejiang University of TechnologyHangzhouChina

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