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Bacterial Community Features Are Shaped by Geographic Location, Physicochemical Properties, and Oil Contamination of Soil in Main Oil Fields of China

  • Environmental Microbiology
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Abstract

Geographic location and physicochemical properties are thought to represent major factors that shape soil bacterial community abundance and diversity. Crude oil contamination is becoming a notable concern with respect to soil property variation; however, the quantifiable influences of geographic location, physicochemical properties, and oil contamination are still poorly understood. In this study, the 16S ribosomal RNA genes of bacteria in the four oil fields in China were analyzed by using pyrosequencing. Results showed that physicochemical properties were the most dominant factor of bacterial community distribution, followed by geographical location. Oil contamination was a driving factor whose indirect influence was stronger than its direct influence. Under the impact of these three factors, different oil fields presented diversified and distinguishable bacterial community features. The soil of sites with the highest total petroleum hydrocarbon content (HB), nitrogen content (DQ), and phosphorus content (XJ) contained the largest proportion of functional groups participating in hydrocarbon degradation, nitrogen turnover, and phosphorus turnover, respectively. The first dominant phylum of the site with loam soil texture (HB) was Actinobacteria instead of Proteobacteria in other sites with sandy or sandy loam soil texture (DQ, SL, XJ). The site with the highest salinization and alkalization (SL) exhibited the largest proportion of unique local bacteria. The site that was located in the desert with extremely low precipitation (XJ) had the most diversified bacteria distribution. The bacterial community diversity was strongly influenced by soil physicochemical properties.

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References

  1. Maier RM, Pepper IL, Gerba CP (eds) (2009) Environmental microbiology (Vol. 397). Academic Press, San Diego

  2. Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5(3):240–245

    Article  CAS  PubMed  Google Scholar 

  3. Fulthorpe RR, Roesch LF, Riva A, Triplett EW (2008) Distantly sampled soils carry few species in common. ISME J 2(9):901–910

    Article  CAS  PubMed  Google Scholar 

  4. Gerdes B, Brinkmeyer R, Dieckmann G, Helmke E (2005) Influence of crude oil on changes of bacterial communities in Arctic sea‐ice. FEMS Microbiol Ecol 53(1):129–139

    Article  CAS  PubMed  Google Scholar 

  5. Fierer N, Nemergut D, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642

    Article  PubMed  Google Scholar 

  6. Banning NC, Gleeson DB, Grigg AH, Grant CD, Andersen GL et al (2011) Soil microbial community successional patterns during forest ecosystem restoration. Appl Environ Microbiol 77:6158–6164

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Ding G, Piceno YM, Heuer H, Weinert N (2013) Changes of soil bacterial diversity as a consequence of agricultural land use in a semi-arid ecosystem. PLoS One 8:e59497

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Zhang Y, Cong J, Lu H, Yang C, Yang Y, Zhou J, Li D (2014) An integrated study to analyze soil microbial community structure and metabolic potential in two forest types. PLoS One 9(4):e93773

    Article  PubMed Central  PubMed  Google Scholar 

  9. Allen JP, Atekwana EA, Atekwana EA, Duris JW, Werkema DD, Rossbach S (2007) The microbial community structure in petroleum-contaminated sediments corresponds to geophysical signatures. Appl Environ Microbiol 73(9):2860–2870

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Paissé S, Coulon F, Goñi‐Urriza M, Peperzak L, McGenity TJ, Duran R (2008) Structure of bacterial communities along a hydrocarbon contamination gradient in a coastal sediment. FEMS Microbiol Ecol 66(2):295–305

    Article  PubMed  Google Scholar 

  11. Yang YY, Wang J, Liao JQ, Huang Y, Xie SG (2014) Distribution of naphthalene dioxygenase genes in crude oil-contaminated soils. Microb Ecol. doi:10.1007/s00248-014-0457-7

    PubMed Central  Google Scholar 

  12. Khamehchiyan M, Hossein Charkhabi A, Tajik M (2007) Effects of crude oil contamination on geotechnical properties of clayey and sandy soils. Eng Geol 89(3):220–229

    Article  Google Scholar 

  13. Al Dousari A, Literathy P (2008) Evidence of hydrocarbon contamination from the Burgan oil field, Kuwait—interpretations from thermal remote sensing data. J Environ Manag 86(4):605–615

    Article  Google Scholar 

  14. Gogoi BK, Dutta NN, Goswami P, Krishna Mohan TR (2003) A case study of bioremediation of petroleum-hydrocarbon contaminated soil at a crude oil spill site. Adv Environ Res 7(4):767–782

    Article  CAS  Google Scholar 

  15. Hamid HRA, Kassim WM, El Hishir A, El-Jawashi SA (2008) Risk assessment and remediation suggestion of impacted soil by produced water associated with oil production. Environ Monit Assess 145(1–3):95–102

    Article  Google Scholar 

  16. Liang Y, Van Nostrand JD, Deng Y, He Z, Wu L, Zhang X et al (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 

  17. 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 

  18. 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 

  19. China Meteorological Data Sharing Service System (2012) http://jingyan.baidu.com/article/fa4125ac906aa328ac7092d6.html. Accessed 30 Dec 2012

  20. 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 

  21. ASTM D4124–01 (2001) Standard test methods for separation of asphalt into four fractions. ASTM International, West Conshohocken

    Google Scholar 

  22. Lu RK (1999) Soil agricultural chemical analysis. China agricultural science and technology press, Nanjing

    Google Scholar 

  23. Al-Mailem D, Sorkhoh N, Al-Awadhi H, Eliyas M, Radwan S (2010) Biodegradation of crude oil and pure hydrocarbons by extreme halophilic archaea from hypersaline coasts of the Arabian Gulf. Extremophiles 14:321–328

    Article  CAS  PubMed  Google Scholar 

  24. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437(7057):376–380

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. 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  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. ter Braak CJ and Smilauer P (1998) CANOCO reference manual and user’s guide to Canoco for Windows: software for canonical community ordination (version 4)

  30. McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities (Vol. 28). MjM software design, Gleneden Beach

    Google Scholar 

  31. Chen H (2011) VennDiagram: Generate high-resolution Venn and Euler plots. R package version, 113

  32. Kolde R (2012) pheatmap: pretty heatmaps. R package version, 61

  33. 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 Microbiol 51(6):1965–1968

    Article  CAS  PubMed  Google Scholar 

  34. 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 

  35. 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 Microbiol 53(4):1155–1163

    Article  CAS  PubMed  Google Scholar 

  36. 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  CAS  PubMed Central  PubMed  Google Scholar 

  37. 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 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  40. Magot M, Ollivier B, Patel BK (2000) Microbiology of petroleum reservoirs. Antonie Van Leeuwenhoek 77(2):103–116

    Article  CAS  PubMed  Google Scholar 

  41. 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 

  42. Yakimov MM, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN et al (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 

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

    Article  CAS  PubMed  Google Scholar 

  44. 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 

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

    Article  CAS  Google Scholar 

  46. 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 

  47. 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 Microbiol 50(6):2083–2092

    Article  CAS  PubMed  Google Scholar 

  48. 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 

  49. Pignatello JJ, Xing B (1996) Mechanisms of slow sorption of organic chemicals to natural particles. Environ Sci Technol 30(1):1–11

    Article  CAS  Google Scholar 

  50. Zhou E, Crawford RL (1995) Effects of oxygen, nitrogen, and temperature on gasoline biodegradation in soil. Biodegradation 6(2):127–140

    Article  CAS  PubMed  Google Scholar 

  51. Zhou J, Kang S, Schadt CW, Garten CT (2008) Spatial scaling of functional gene diversity across various microbial taxa. Proc Natl Acad Sci U S A 105(22):7768–7773

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Ramette A, Tiedje JM (2007) Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem. Proc Natl Acad Sci U S A 104(8):2761–2766

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Bhattacharya D, Sarma PM, Krishnan S, Mishra S, Lal B (2003) Evaluation of genetic diversity among Pseudomonas citronellolis strains isolated from oily sludge-contaminated sites. Appl Environ Microbiol 69(3):1435–1441

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. He J, Xu Z, Hughes J (2006) Molecular bacterial diversity of a forest soil under residue management regimes in subtropical Australia. FEMS Microbiol Ecol 55(1):38–47

    Article  CAS  PubMed  Google Scholar 

  55. Rooney-Varga JN, Giewat MW, Duddleston KN, Chanton JP, Hines ME (2007) Links between archaeal community structure, vegetation type and methanogenic pathway in Alaskan peatlands. FEMS Microbiol Ecol 60(2):240–251

    Article  CAS  PubMed  Google Scholar 

  56. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72(3):1719–1728

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3(8):992–1000

    Article  CAS  PubMed  Google Scholar 

  58. Paerl HW, Dyble J, Moisander PH, Noble RT, Piehler MF, Pinckney JL et al (2003) Microbial indicators of aquatic ecosystem change: current applications to eutrophication studies. FEMS Microbiol Ecol 46(3):233–246

    Article  CAS  PubMed  Google Scholar 

  59. 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 

  60. Akkermans AD, Van Elsas JD, De Bruijn FJ (1995) Molecular microbial ecology manual. Kluwer, Dordrecht, pp 1–8

    Book  Google Scholar 

  61. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75(15):5111–5120

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Bachar A, Al-Ashhab A, Soares MIM, Sklarz MY, Angel R, Ungar ED, Gillor O (2010) Soil microbial abundance and diversity along a low precipitation gradient. Microb Ecol 60(2):453–461

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Public Welfare Project of Ministry of Environmental Protection (No. 201309034).

Conflict of Interest

The authors declare that there is no conflict of interests regarding the publication of this article.

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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, Haidian District, Beijing, 100871, People’s Republic of China

    Jingqiu Liao, Jie Wang & Yi Huang

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  1. Jingqiu Liao
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  2. Jie Wang
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  3. Yi Huang
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Correspondence to Yi Huang.

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Table S1

Most abundant 20 genera identified in the four oil fields (DOC 55 kb)

Table S2

Functional groups and their taxonomy (DOC 73 kb)

Table S3

Pearson’s correlation matrix of contamination factor alternative index (DOC 30 kb)

Table S4

Pearson’s correlation matrix of basic soil physicochemical index and contaminant (DOC 41 kb)

Table S5

Pearson’s correlation matrix of physicochemical factor alternative index (DOC 46 kb)

Table S6

The pair Jaccard similarity of bacterial community (DOC 30 kb)

Figure S1

Schematic map of sampling sites (DOC 1106 kb)

Figure S2

Venn diagram showing the unique and shared OTUs0.03 (DOC 422 kb)

Figure S3

Distribution of the top 40 most abundant classes of bacteria found in contaminated soil in research areas (DOC 196 kb)

Figure S4

Physicochemical PCA of contaminated and uncontaminated soil (DOC 46 kb)

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Liao, J., Wang, J. & Huang, Y. Bacterial Community Features Are Shaped by Geographic Location, Physicochemical Properties, and Oil Contamination of Soil in Main Oil Fields of China. Microb Ecol 70, 380–389 (2015). https://doi.org/10.1007/s00248-015-0572-0

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