Skip to main content

Advertisement

SpringerLink
Log in

Long-term oil contamination causes similar changes in microbial communities of two distinct soils

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Since total petroleum hydrocarbons (TPH) are toxic and persistent in environments, studying the impact of oil contamination on microbial communities in different soils is vital to oil production engineering, effective soil management and pollution control. This study analyzed the impact of oil contamination on the structure, activity and function in carbon metabolism of microbial communities of Chernozem soil from Daqing oil field and Cinnamon soil from Huabei oil field through both culture-dependent techniques and a culture-independent technique—pyrosequencing. Results revealed that pristine microbial communities in these two soils presented disparate patterns, where Cinnamon soil showed higher abundance of alkane, (polycyclic aromatic hydrocarbons) PAHs and TPH degraders, number of cultivable microbes, bacterial richness, bacterial biodiversity, and stronger microbial activity and function in carbon metabolism than Chernozem soil. It suggested that complicated properties of microbes and soils resulted in the difference in soil microbial patterns. However, the changes of microbial communities caused by oil contamination were similar in respect of two dominant phenomena. Firstly, the microbial community structures were greatly changed, with higher abundance, higher bacterial biodiversity, occurrence of Candidate_division_BRC1 and TAO6, disappearance of BD1-5 and Candidate_division_OD1, dominance of Streptomyces, higher percentage of hydrocarbon-degrading groups, and lower percentage of nitrogen-transforming groups. Secondly, microbial activity and function in carbon metabolism were significantly enhanced. Based on the characteristics of microbial communities in the two soils, appropriate strategy for in situ bioremediation was provided for each oil field. This research underscored the usefulness of combination of culture-dependent techniques and next-generation sequencing techniques both to unravel the microbial patterns and understand the ecological impact of contamination.

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

  • Almeida R, Mucha AP, Teixeira C, Bordalo AA, Almeida CM (2013) Biodegradation of petroleum hydrocarbons in estuarine sediments: metal influence. Biodegradation 24:111–123

    Article  CAS  PubMed  Google Scholar 

  • ASTM(American Society for Testing and Materials) D4124–01 (2001) Standard test methods for separation of asphalt into four fractions. ASTM International, West Conshohocken

    Google Scholar 

  • Bent SJ, Pierson JD, Forney LJ (2007) Measuring species richness based on microbial community fingerprints: the emperor has no clothes. Appl Environ Microbiol 73:2399–2401

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berthe-Corti L, Höpner T (2005) Geo-biological aspects of coastal oil pollution. Palaeogeogr Palaeocl 219(1):171–189

    Article  Google Scholar 

  • Berthrong ST, Buckley DH, Drinkwater LE (2013) Agricultural management and labile carbon additions affect soil microbial community structure and interact with carbon and nitrogen cycling. Microb Ecol 66(1):158–170

    Article  CAS  PubMed  Google Scholar 

  • Bordoloi NK, Konwar BK (2009) Bacterial biosurfactant in enhancing solubility and metabolism of petroleum hydrocarbons. J Hazard Mater 170(1):495–505

    Article  CAS  PubMed  Google Scholar 

  • Brito EMS, Guyoneaud R, Goñi-Urriza M, Ranchou-Peyruse A, Verbaere A, Crapez MA, Wasserman JCA, Duran R (2006) Characterization of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara Bay. Brazil Res Microbiol 157(8):752–762

    Article  CAS  PubMed  Google Scholar 

  • Camargo FAO, Bento FM, Okeke BC, Frankenberger WT (2004) Hexavalent chromium reduction by an actinomycete, Arthrobacter crystallopoietes ES 32. Biol Trace Elem Res 97(2):183–194

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chin KJ, Liesack W, Janssen PH (2001) Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division ‘Verrucomicrobia’ isolated from rice paddy soil. Int J Syst Evol Micr 51(6):1965–1968

    Article  CAS  Google Scholar 

  • China Meteorological Data Sharing Service System. (2012). http://jingyan.baidu.com/article/fa4125ac906aa328ac7092d6.html.

  • Choi KH, Dobbs FC (1999) Comparison of two kinds of Biolog microplates(GN and ECO) in their ability to distinguish among aquatic microbial communities. J Microbiol Meth 36(3):203–213

    Article  CAS  Google Scholar 

  • DeBruyn JM, Nixon LT, Fawaz MN, Johnson AM, Radosevich M (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microbiol 77(17):6295–6300

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ding GC, Heuer H, Zühlke S, Spiteller M, Pronk GJ, Heister K, Kögel-Knabner I, Smalla K (2010) Soil type-dependent responses to phenanthrene as revealed by determining the diversity and abundance of polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenase genes by using a novel PCR detection system. Appl Environ Microbiol 76(14):4765–4771

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ding GC, Heuer H, Smalla K (2012) Dynamics of bacterial communities in two unpolluted soils after spiking with phenanthrene: soil type specific and common responders. Front Microbiol 3:1–11

    Article  Google Scholar 

  • Dos Santos HF, Cury JC, Do Carmo FL, Dos Santos AL, Tiedje J, Van Elsas JD, Rosado AS, Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS One 6:e16943. doi:10.1371/journal.pone.0016943

    Article  PubMed Central  PubMed  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461

    Article  CAS  PubMed  Google Scholar 

  • F.A.O. (2006) World references base for soil resources. World Soil Resource Reports 103. FAO, Rome

    Google Scholar 

  • Fine P, Graber ER, Yaron B (1997) Soil interactions with petroleum hydrocarbons: abiotic processes. Soil Technol 10(2):133–153

    Article  Google Scholar 

  • Foght J, Aislabie J (2005) Enumeration of soil microorganisms. In: Margesin R, Schinner F (eds) Manual for Soil Analysis – Monitoring and Assessing Soil Bioremediation. Springer, Berlin, Heidelberg, Germany, pp 261–280

    Chapter  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57(8):2351–2359

    PubMed Central  CAS  PubMed  Google Scholar 

  • Greenwood PF, Wibrow S, George SJ, Tibbett M (2009) Hydrocarbon biodegradation and soil microbial community response to repeated oil exposure. Org Geochem 40(3):293–300

    Article  CAS  Google Scholar 

  • Gu J, Cai H, Yu SL, Qu R, Yin B, Guo YF, Zhao JY, Wu XL (2007) Marinobacter gudaonensis sp. nov., isolated from an oil-polluted saline soil in a Chinese oilfield. Int J Syst Evol Micr 57(2):250–254

    Article  CAS  Google Scholar 

  • Guo H, Yao J, Cai M, Qian Y, Guo Y, Richnow HH, Blake RE, Doni S, Ceccanti B (2012) Effects of petroleum contamination on soil microbial numbers, metabolic activity and urease activity. Chemosphere 87(11):1273–1280

    Article  CAS  PubMed  Google Scholar 

  • Haines JR, Wrenn BA, Holder EL, Strohmeier KL, Herrington RT, Venosa AD (1996) Measurement of hydrocarbon-degrading microbial populations by a 96-well plate most-probable-number procedure. J Ind Microbiol Biot 16(1):36–41

    Article  CAS  Google Scholar 

  • Hara A, Syutsubo K, Harayama S (2003) Alcanivorax which prevails in oil-contaminated seawater exhibits broad substrate specificity for alkane degradation. Environ Microbiol 5(9):746–753

    Article  CAS  PubMed  Google Scholar 

  • Head IM, Jones DM, Röling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4(3):173–182

    Article  CAS  PubMed  Google Scholar 

  • Huesemann M (1995) Predictive model for estimating the extent of petroleum hydrocarbon biodegradation in contaminated soils. Environ Sci Technol 29:7–18

    Article  CAS  PubMed  Google Scholar 

  • Insam H, Rangger A (1997) Microbial communities: functional versus structural approaches. Springer, Berlin, Heidelberg, New York

    Book  Google Scholar 

  • Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182(8):2059–2067

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaufmann K, Christophersen M, Buttler A, Harms H, Höhener P (2004) Microbial community response to petroleum hydrocarbon contamination in the unsaturated zone at the experimental field site Værløse, Denmark. FEMS Microbiol Ecol 48(3):387–399

    Article  CAS  PubMed  Google Scholar 

  • Kolde, R. (2012). Pheatmap: Pretty Heatmaps. R package version, 61

  • Lennon JT (2011) Replication, lies and lesser-known truths regarding experimental design in environmental microbiology. Environ Microbiol 13:1383–1386

    Article  PubMed  Google Scholar 

  • Li G, Huang W, Lerner DN, Zhang X (2000) Enrichment of degrading microbes and bioremediation of petrochemical contaminants in polluted soil. Water Res 34(15):3845–3853

    Article  CAS  Google Scholar 

  • Liang Y, Van Nostrand JD, Deng Y, He Z, Wu L, Zhang X, Li GH, Zhou J (2011) Functional gene diversity of soil microbial communities from five oil-contaminated fields in China. ISME J 5(3):403–413

    Article  PubMed Central  PubMed  Google Scholar 

  • Liao, J. Q., Wang, J., Huang, Y. (2015). Bacterial community features are shaped by geographic location, physicochemical properties and oil contamination of soil in main oil fields of China. Microb. Ecol. DOI 10.1007/s00248-015-0572-0

  • Liu YJ, Chen YP, Jin PK, Wang XC (2009) Bacterial communities in a crude oil gathering and transferring system (China). Anaerobe 15(5):214–218

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Yang H, Zhao M, Zhang XH (2014) Spatial distribution patterns of benthic microbial communities along the Pearl Estuary. China Syst Appl Microbiol 37:578–589

    Article  PubMed  Google Scholar 

  • Lu RK (1999) Soil agricultural chemical analysis. China Agricultural Science and Technology Press, Nanjing, China

    Google Scholar 

  • Magot M, Ollivier B, Patel BK (2000) Microbiology of petroleum reservoirs. Anton Leeuw 77(2):103–116

    Article  CAS  Google Scholar 

  • Margesin R, Labbe D, Schinner F, Greer CW, Whyte LG (2003) Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Appl Environ Microbiol 69(6):3085–3092

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Margesin R, Hammerle 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 53:259–269

    Article  CAS  PubMed  Google Scholar 

  • Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437(7057):376–380

    PubMed Central  CAS  PubMed  Google Scholar 

  • Oh YS, Sim DS, Kim SJ (2001) Effects of nutrients on crude oil biodegradation in the upper intertidal zone. Mar Pollut Bull 42(12):1367–1372

    Article  CAS  PubMed  Google Scholar 

  • Paerl HW, Dyble J, Moisander PH, Noble RT, Piehler MF, Pinckney JL, Steppe TF, Twomey L, Valdes LM (2003) Microbial indicators of aquatic ecosystem change: current applications to eutrophication studies. FEMS Microbiol Ecol 46(3):233–246

    Article  CAS  PubMed  Google Scholar 

  • Powell SM, Bowman JP, Snape I, Stark JS (2003) Microbial community variation in pristine and polluted nearshore Antarctic sediments. FEMS Microbiol Ecol 45(2):135–145

    Article  CAS  PubMed  Google Scholar 

  • Powell SM, Bowman JP, Ferguson SH, Snape I (2010) The importance of soil characteristics to the structure of alkane-degrading bacterial communities on sub-Antarctic Macquarie Island. Soil Biol Biochem 42(11):2012–2021

    Article  CAS  Google Scholar 

  • Prosser JI (2010) Replicate or lie. Environ Microbiol 12:1806–1810

    Article  CAS  PubMed  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35(21):7188–7196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Radwan SS, Barabás G, Sorkhoh NA, Damjanovich S, Szabó I, Szöllősi J, Matkó J, Penyige A, Hirano T, Szabó IM (1998) Hydrocarbon uptake by Streptomyces. FEMS Microbiol Lett 169(1):87–94

    Article  CAS  PubMed  Google Scholar 

  • Radwan SS, Al-Hasan RH, Ali N, Salamah S, Khanafer M (2005) Oil-consuming microbial consortia floating in the Arabian Gulf. Int Biodeter Biodegr 56(1):28–33

    Article  CAS  Google Scholar 

  • Ribeiro H, Mucha AP, Marisa R, Almeida C, Bordalo AA (2013) Bacterial community response to petroleum contamination and nutrient addition in sediments from a temperate salt marsh. Sci Total Environ 458:568–576

    Article  PubMed  Google Scholar 

  • Santos, H. F., Carmo, F. L., Paes, J. E. S., Rosado, A. S., Peixoto, R. S. (2010). Bioremediation of mangroves impacted by petroleum. Water Air Soil Poll. DOI: 10.1007/s11270-010-0536-4.

  • Saul DJ, Aislabie JM, Brown CE, Harris L, Foght JM (2005) Hydrocarbon contamination changes the bacterial diversity of soil from around Scott Base, Antarctica. FEMS Microbiol Ecol 53(1):141–155

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smetia E, Ar Kormasb K, Spatharis S (2013) A non-phylogenetic alpha diversity approach on prokaryotic community structure in aquatic systems. Ecol Indic 29:361–366

    Article  Google Scholar 

  • Sorkhoh N, Al-Hasan R, Radwan S (1992) Self-cleaning of the Gulf. Nature 359:109

    Article  Google Scholar 

  • Sutton NB, Maphosa F, Morillo JA, Abu Al-Soud W, Langenhoff AA, Grotenhuis T, Rijnaarts HH, Smidt H (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79(2):619–630

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tian Y, Luo YR, Zheng TL, Cai LZ, Cao XX, Yan CL (2008) Contamination and potential biodegradation of polycyclic aromatic hydrocarbons in mangrove sediments of Xiamen. China Mar Pollut Bull 56:1184–1191

    Article  CAS  PubMed  Google Scholar 

  • Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol R 67(4):503–549

    Article  Google Scholar 

  • Wang, J., Cao, X. F., Liao, J. Q., Huang, Y., Tang, X. Y. (2014). Carcinogenic potential of PAHs in oil-contaminated soils from the main oil fields across China. Environ Sci Pollut R, DOI 10.1007/s11356-014-3954-9

  • Westerberg K, Elväng AM, Stackebrandt E, Jansson JK (2000) Arthrobacter chlorophenolicus sp. nov. a new species capable of degrading high concentrations of 4-chlorophenol. Int J Syst Evol Micr 50(6):2083–2092

    Article  CAS  Google Scholar 

  • Wrenn BA, Venosa AD (1996) Selective enumeration of aromatic and aliphatic hydrocarbon degrading bacteria by a most-probable-number procedure. Can J Microbiol 42(3):252–258

    Article  CAS  PubMed  Google Scholar 

  • Yakimov MM, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN, Timmis KN, Golyshin PN, Giluliano L (2005) Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol 7(9):1426–1441

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y. Y., Wang, J., Liao, J. Q., Huang, Y., Xie, S. G. (2014). Distribution of naphthalene dioxygenase genes in crude oil-contaminated soils. Microb. Ecol. DOI 10.1007/s00248-014-0457-7

  • Zak JC, Willig MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26(9):1101–1108

    Article  Google Scholar 

  • Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov. a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Micr 53(4):1155–1163

    Article  CAS  Google Scholar 

  • Zhu X, Venosa A, Makram T, Lee K (2004) Guidelines for the bioremediation of oil contaminated salt marshes. EPA/600/R-04/074. US Environmental Protection Agency, Cincinnati

    Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflicts of interest.

Funding

This study was funded by Public Welfare Project of Ministry of Environmental Protection (No. 201309034).

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Author information

Authors and Affiliations

  1. State Key Joint Laboratory of Environmental Simulation and Pollution Control, College of Environmental Sciences and Engineering, Peking University, No. 5 Yiheyuan Road, Beijing, Haidian District, 100871, People’s Republic of China

    Jingqiu Liao, Jie Wang, Dalin Jiang & Yi Huang

  2. Department of Mechanical Science and Engineering, University of Illinois at Urbana-Champaign, 1206 W. Green, St., Urbana, IL, 61801, USA

    Michael Cai Wang

Authors
  1. Jingqiu Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dalin Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael Cai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yi Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yi Huang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 241 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liao, J., Wang, J., Jiang, D. et al. Long-term oil contamination causes similar changes in microbial communities of two distinct soils. Appl Microbiol Biotechnol 99, 10299–10310 (2015). https://doi.org/10.1007/s00253-015-6880-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6880-y

Keywords

Search

Navigation