Environmental Science and Pollution Research

, Volume 24, Issue 8, pp 7139–7159 | Cite as

Metagenomic insights into effects of spent engine oil perturbation on the microbial community composition and function in a tropical agricultural soil

  • Lateef B. SalamEmail author
  • Sunday O. Obayori
  • Francisca O. Nwaokorie
  • Aisha Suleiman
  • Raheemat Mustapha
Research Article


Analyzing the microbial community structure and functions become imperative for ecological processes. To understand the impact of spent engine oil (SEO) contamination on microbial community structure of an agricultural soil, soil microcosms designated 1S (agricultural soil) and AB1 (agricultural soil polluted with SEO) were set up. Metagenomic DNA extracted from the soil microcosms and sequenced using Miseq Illumina sequencing were analyzed for their taxonomic and functional properties. Taxonomic profiling of the two microcosms by MG-RAST revealed the dominance of Actinobacteria (23.36%) and Proteobacteria (52.46%) phyla in 1S and AB1 with preponderance of Streptomyces (12.83%) and Gemmatimonas (10.20%) in 1S and Geodermatophilus (26.24%), Burkholderia (15.40%), and Pseudomonas (12.72%) in AB1, respectively. Our results showed that soil microbial diversity significantly decreased in AB1. Further assignment of the metagenomic reads to MG-RAST, Cluster of Orthologous Groups (COG) of proteins, Kyoto Encyclopedia of Genes and Genomes (KEGG), GhostKOALA, and NCBI’s CDD hits revealed diverse metabolic potentials of the autochthonous microbial community. It also revealed the adaptation of the community to various environmental stressors such as hydrocarbon hydrophobicity, heavy metal toxicity, oxidative stress, nutrient starvation, and C/N/P imbalance. To the best of our knowledge, this is the first study that investigates the effect of SEO perturbation on soil microbial communities through Illumina sequencing. The results indicated that SEO contamination significantly affects soil microbial community structure and functions leading to massive loss of nonhydrocarbon degrading indigenous microbiota and enrichment of hydrocarbonoclastic organisms such as members of Proteobacteria and Actinobacteria.


Spent engine oil Agricultural soil Soil microcosm Illumina sequencing Microbial community structure Hydrocarbon degradation 

Supplementary material

11356_2017_8364_MOESM1_ESM.docx (192 kb)
Figure S1 Comparative taxonomic profile of the 1S and AB1 microcosms at order level, computed by MG-RAST. Only orders with significant biological differences (P < 0.05, difference between the proportions >1% and twofold of ratio between the proportions, as determined by STAMP) (DOCX 192 kb)
11356_2017_8364_MOESM2_ESM.docx (187 kb)
Figure S2 Comparative taxonomic profile of the 1S and AB1 microcosms at family level, computed by MG-RAST. Only families with significant biological differences (P < 0.05, difference between the proportions >1% and twofold of ratio between the proportions, as determined by STAMP) (DOCX 187 kb).
11356_2017_8364_MOESM3_ESM.docx (29 kb)
Figure S3 Functional characterization of metagenomic sequencing reads of Agricultural soil 1S microcosm according to the Cluster of Orthologous Groups of protein (COGs). The categories for COG are abbreviated as follows: C: energy production and conversion; E: amino acid transport and metabolism; F: nucleotide transport and metabolism; G: carbohydrate transport and metabolism; H: coenzyme transport and metabolism; I: lipid transport and metabolism; D: cell cycle control, cell division, chromosome partitioning; N: cell motility; T: signal transduction mechanism; U: intracellular trafficking, secretion and vesicular transport; V: defense mechanisms; K: transcription; L: replication, recombination and repair; R: general function prediction only; S: function unknown (DOCX 29 kb).


  1. Abdulsalam S, Adefila SS, Bugaje IM, Ibrahim S (2012) Bioremediation of soil contaminated with used motor oil in a closed system. Bioremediation and biodegradation. J Bioremed Biodeg 3:12. doi: 10.4172/2155-6199.1000172 Google Scholar
  2. Abed RM, Al-Kindi S, Al-Kharusi S (2015) Diversity of bacterial communities along a petroleum contamination gradient in desert soils. Microb Ecol 69(1):95–105CrossRefGoogle Scholar
  3. Adebusoye SA, Ilori MO, Amund OO, Teniola OO, Olatope SO (2007) Microbial degradation of petroleum in a polluted tropical stream. World J Microbiol Biotechnol 23:1149–1159Google Scholar
  4. Adelowo OO, Alagbe SO, Ayandele AA (2006) Time-dependent stability of used engine oil degradation by cultures of Pseudomonas fragi and Achromobacter aerogenes. Afri J Biotechnol 5:3476–2479Google Scholar
  5. Alyward FO, McDonald BR, Adams SM et al (2013) Comparison of 26 Sphingomonad genomes reveals diverse environmental adaptations and biodegradative capabilities. Appl Environ Microbiol 79:3724–3733CrossRefGoogle Scholar
  6. Andrew RWJ, Jackson JM (1996) Environmental science: the natural environment and human impact. Longman Publishers, SingaporeGoogle Scholar
  7. Atlas RM (1981) Microbial degradation of petroleum: an environmental perspective. Microbiol Rev 45:180–209Google Scholar
  8. Atlas RM (1991) Microbial hydrocarbon degradation: bioremediation of oil spills. J Chem Technol Biotechnol 52:149–156CrossRefGoogle Scholar
  9. Bagherzadeh-Namazi A, Shojaosadati SA, Hashemi-Najafabadi S (2008) Biodegradation of used engine oil using mixed and isolated cultures. Int J Environ Res 2:431–440Google Scholar
  10. Balkwill DL, Fredrickson JK, Romine MF (2006) Sphingomonas and related genera. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds.), The Prokaryotes: Springer New York, pp. 605–629Google Scholar
  11. Baraniecki CA, Aislabie J, Foght JM (2002) Characterization of Sphingomonas sp. ant 17, an aromatic hydrocarbon-degrading bacterium isolated from Antarctic soil. Microb Ecol 43:44–54CrossRefGoogle Scholar
  12. Bashir Y, Singh SP, Konwar BK (2014) Metagenomics: an application-based perspective. Chinese J Biol. doi: 10.1155/2014/1460301-7. Google Scholar
  13. Basuki W, Syahputra K, Suryani AT, Pradipta I (2011) Biodegradation of used engine oil. Indonesian J Biotechnol 16:132–138Google Scholar
  14. Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917CrossRefGoogle Scholar
  15. Bell TH, Yergeau E, Maynard C, Juck C, Whyte LG, Greer CW (2013) Predictable bacterial composition and hydrocarbon degradation in artic soils following diesel and nutrient disturbance. The ISME journals 7:1200–1210CrossRefGoogle Scholar
  16. Bestawy E, Mohamed H, Nawal E (2005) The potentiality of free gram-negative bacteria for removing oil and grease from contaminated industrial effluents. World J Microbiol Biotechnol 21:815–822CrossRefGoogle Scholar
  17. Bundy JG, Paton GI, Campbell CD (2002) Microbial communities in different soils do not converge after diesel contamination. J Appl Microbiol 92:276–288Google Scholar
  18. Cheung PY, Kinkle BK (2001) Mycobacterium diversity and pyrene mineralization in petroleumcontaminated soils. Appl Environ Microbiol 67:2222–2229Google Scholar
  19. Cooksey DA (1994) Molecular mechanisms for copper resistance and accumulation in bacteria. FEMS Microbiol Rev 14:381–386CrossRefGoogle Scholar
  20. Dalal J, Sarma PM, Lavania M, Mandal AK, Lal B (2010) Evaluation of bacterial strains isolated from oil-contaminated soil for production of polyhydroxyalkanoic acids (PHA). Pedobiologia 54:25–30CrossRefGoogle Scholar
  21. Dominguez-Rusado E, Pitchel J (2003) Chemical characterization of fresh and weathered motor oil via GC/MS, NMR and FITR Techniques. Proceedings of the Indiana Academy of Science 112: 109–116Google Scholar
  22. 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 6Google Scholar
  23. Endo G, Narita M, Huang CC, Silver S (2002) Microbial heavy metal resistance transposons and plasmids: potential use for environmental biotechnology. J Environ Biotechnol 2:71–82Google Scholar
  24. Esser D, Kouril T, Talfournier F et al (2013) Unravelling the function of paralogs of the aldehyde dehydrogenase super family from Sulfolobus solfataricus. Extremophiles 12:75–88Google Scholar
  25. Fuentes S, Barra B, Caporaso G, Seeger M (2016) From rare to dominant: a fine-tuned soil bacterial bloom during petroleum hydrocarbon bioremediation. Appl Environ Microbiol 82(3):888–896CrossRefGoogle Scholar
  26. George KW, Hay AG (2011) Bacterial strategies for growth on aromatic compounds. Adv Appl Microbiol 74:1–33CrossRefGoogle Scholar
  27. Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9(7):1613–1631CrossRefGoogle Scholar
  28. Greer CW, Whyte LG, Niederberger TD (2010) Microbial communities in hydrocarbon-contaminated temperate, tropical alpine, and polar soils. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer-Verlag, Berlin, pp 2313–2328CrossRefGoogle Scholar
  29. Gtari M, Essoussi I, Maaoui R et al (2012) Contrasted resistance of stone-dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species. FEMS Microbiol Ecol 80(3):566–577CrossRefGoogle Scholar
  30. Habe H, Ashikawa Y, Saiki Y, Yoshida T, Nojiri H, Omori T (2002) Sphingomonas sp strain KA1, carrying a carbazole dioxygenase gene homologue, degrades chlorinated dibenzo-p-dioxins in soil. FEMS Microbiol Lett 211:43–49CrossRefGoogle Scholar
  31. Hagwell IS, Delfino LM, Rao JJ (1992) Partitioning of polycyclic aromatic hydrocarbons from oil into water. Environ Sci Technol 26:2104–2110CrossRefGoogle Scholar
  32. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–668CrossRefGoogle Scholar
  33. Harayama S, Kok M, Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601CrossRefGoogle Scholar
  34. Hirano J, Miyamoto K, Ohta H (2005) Purification and characterization of the alcohol dehydrogenase with a broad substrate specificity originated from 2-phenylethanol-assimilating Brevibacterium sp. KU 1309. J Biosci Bioeng 100:318–322CrossRefGoogle Scholar
  35. Ilori MO, Amund OO, Obayori OS, Omotayo AE (2015) Microbial population and physico-chemical dynamics of a soil ecosystem upon petroleum contamination. J Sci Res Dev 15:25–33Google Scholar
  36. Jayashree R, Evany NS, Rajesh PP, Krishnaraju M (2012) Biodegradation capability of bacterial species isolated from oil contaminated soils. J Acad Indus Res 1:140–143Google Scholar
  37. Jin L, Lee H-G, Kim H-S, Ahn C-Y, Oh H-M (2013) Geodermatophilus soli sp. nov. and Geodermatophilus terrae sp. nov., two actinobacteria isolated from grass soil. Int J Syst Evol Microbiol 63(7):2625–2629CrossRefGoogle Scholar
  38. Jurelevicius D, Alvare VM, Marques JM, Lima LRFS, Pias F d A, Seldin L (2013) Bacterial community response to petroleum hydrocarbon amendments in fresh water, marine and hypersaline water- containing microcosms. Appl Environ Microbiol 79(19):5927–5935CrossRefGoogle Scholar
  39. Kanaly RA, Harayama S (2010) Advances in the field of high molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microbiol Biotechnol 3:132–164CrossRefGoogle Scholar
  40. Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428(4):726–731CrossRefGoogle Scholar
  41. Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19CrossRefGoogle Scholar
  42. Kielak AM, Bareto CC, Kowalchuk GA, van Veen JA, Kuramae EC (2016) The ecology of Acidobacteria: Moring beyond genes and genomes. Frontier in Microbiology. doi: 10.3389/fmicb.2016.0074 Google Scholar
  43. Kilndworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41(1):1–11CrossRefGoogle Scholar
  44. Koma D, Sakashita Y, Kubota K et al (2003) Degradation of car engine base oil by Rhodococcus sp. NDKK48 and Gordonia sp. NDKY76A. Biosci Biotechnol Biochem 67:1590–1593CrossRefGoogle Scholar
  45. Kostka JE, Prakash O, Overholt WA et al (2011) Hydrocarbon degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater horizon oil spill. Appl Environ Microbiol 77:7962–7974CrossRefGoogle Scholar
  46. Kunze M, Zerlin KF, Retzlaff A et al (2009) Degradation of chloroaromatics by Pseudomonas putida GJ31: assembled route for chlorobenzene degradation encoded by clusters on plasmid pKW1 and the chromosome. Microbiol 155:4069–4083CrossRefGoogle Scholar
  47. Labbe D, Margesin R, Schinner F, Whyte LG, Greer CW (2007) Comparative phylogenetic analysis of microbial communities in pristine and hydrocarbon-contaminated alpine soils. FEMS Microbiol Ecol 59:466–475CrossRefGoogle Scholar
  48. Lai Q, Li W, Shao Z (2012) Complete genome sequence of Alkanivorax dieselolei type strain B5. J Bacteriol 194:6674CrossRefGoogle Scholar
  49. Larkin MJ, Kulakov LA, Allen CC (2005) Biodegradation and Rhodococcus—masters of catabolic versatility. Curr Opin Biotechnol 16:282–290CrossRefGoogle Scholar
  50. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315Google Scholar
  51. Le Borgne S, Paniagua D, Vazquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92CrossRefGoogle Scholar
  52. Liang Y, Li G, Van Nostrans JD, He Z, Wu L, Deng Y, Zhang X, Zhou J (2009) Microarray-based analysis of microbial functional diversity along an oil contamination gradient in oil field. FEMS Microbiol Ecol 70:168–177CrossRefGoogle Scholar
  53. Lin C, Olson BH (1995) Occurrence of cop-like resistance genes among bacteria isolated from a water distribution system. Can J Microbiol 41:642–646CrossRefGoogle Scholar
  54. Lloyd AC, Cackette TA (2001) Diesel engines: environmental impact and control. J Air Waste Manag Assoc 51:809–847CrossRefGoogle Scholar
  55. Lu S-T, Isaac K (2008) Characterization of motor lubricating oils and their oil water partition. Environ Forens 9:295–309CrossRefGoogle Scholar
  56. Mandri T, Lin J (2007) Isolation and characterization of engine oil degrading indigenous microorganism in Kwazulu-Natal, South Africa. Afr J Biotechnol 62:23–26Google Scholar
  57. Marchler-Bauer A, Derbyshire MK, Gonzales NR et al (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(D):222–D226CrossRefGoogle Scholar
  58. Mason JR, Cammack R (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 46:277–305CrossRefGoogle Scholar
  59. Mishra S, Jyot J, Kuhad R, Lal B (2001) Evaluation of inoculum addition to stimulate in situ bioremediation of oily-sludge-contaminated soil. Appl Environ Microbiol 67(4):1675–1681CrossRefGoogle Scholar
  60. Montero-Calasanz MC, Hezbri K, Göker M et al (2015) Description of gamma radiation-resistant Geodermatophilus dictyosporus sp. nov. to accommodate the not validly named Geodermatophilus obscurus subsp. dictyosporus (Luedemann, 1968). Extremophiles 19:77–85CrossRefGoogle Scholar
  61. Myrold DD, Zeglin LH, Jansson JK (2013) The potential of metagenomics approaches for understanding soil microbial processes. Soil Sci Soc Am J 78:3–10CrossRefGoogle Scholar
  62. Nemergut DR, Martin AP, Schmidt SK (2004) Intergon diversity in heavy-metal-contaminated mine tailings and inferences about integron evolution. Appl Environ Microbiol 70:1160–1168CrossRefGoogle Scholar
  63. Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14:186–199CrossRefGoogle Scholar
  64. Nogales B, Moore ERB, Llobert-Brossa E, Rossello-Mora R, Amann R, Timmis KN (2001) Combined use of 16S ribosomal DNA and 16S rRNA to study the bacterial community of polychlorinated biphenyl-polluted soil. Appl Environ Microbiol 67:1874–1884CrossRefGoogle Scholar
  65. Nucifora G, Chu L, Misra TK, Silver S (1989) Cadmium resistance from Staphylococcus aureus plasmid p1258 cadA gene results from cadmium-efflux ATPase. Proc Natl Acad Sci U S A 86:3544–3548CrossRefGoogle Scholar
  66. Obayori OS, Ilori MO, Adebusoye SA, Amund OO, Oyetibo GO (2008) Microbial population changes in tropical agricultural soil experimentally contaminated with crude petroleum. Afr J Biotechnol 7:4512–4520Google Scholar
  67. Obayori OS, Salam LB (2010) Degradation of polycyclic aromatic hydrocarbons: role of plasmids. Sci Res Essays 5(25):4093–4106Google Scholar
  68. Obayori OS, Salam LB, Ogunwumi OS (2014) Biodegradation of fresh and used engine oils by Pseudomonas aeruginosa LP5. J Bioremed Biodegrad 5:213. doi: 10.4172/2/21556199.1000213 CrossRefGoogle Scholar
  69. Odjegba VJ, Sadiq A (2006) Effects of spent engine oil on the growth parameters, chlorophyll and protein level of Amaranthus hybridus L. Nig J Appl Sci 7:1–46Google Scholar
  70. Okoh AI, Trejo-Hernandez MR (2006) Remediation of petroleum hydrocarbon polluted systems: exploiting the bioremediation strategies. Afr J Biotechnol 5(25):2520–2525Google Scholar
  71. Olajire AA, Essien JP (2014) Aerobic degradation of petroleum components by microbial consortia. Petrol Environ Biotechnol 5:5. doi: 10.4172/2157-7463.1000195 Google Scholar
  72. Oulas A, Pavloudi G, Polymanakou P, Pavlopoulus GA, Papanikolaou N, Kotoulas G, Arvanitidis C, Iliopoulus I (2015) Metagenomics: tools and insights for analysing next-generation sequencing data derived from biodiversity studies. Bioinformatics and Biology insights 9:75–88Google Scholar
  73. Outten FW, Outten CE, O’Halloran T (2000) Metalloregulatory systems at the interface between bacterial metal homeostasis and resistance. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM Press, Washington D.C, pp 145–157Google Scholar
  74. Oyetibo GO, Ilori MO, Adebusoye SA, Obayori OS, Amund OO (2010) Bacteria with dual resistance to elevated concentrations of heavy metals and antibiotics in Nigerian contaminated systems. Environ Monit Assess 168:305–314CrossRefGoogle Scholar
  75. Parales RE, Ju KS, Rollefson J, Ditty JL (2008) Bioavailability, transport and chemotaxis of organic pollutants. In: Diaz E (ed) Microbial Bioremediation. Caister Academic Press, Norfolk, pp 145–187Google Scholar
  76. Parks DH, Tyson GW, Hugenhiltz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30(21):3123–3124CrossRefGoogle Scholar
  77. Pathak H, Jaroli BP (2012) Biochemical characterization of 4 t engine oil degrading microorganism isolated from polluted soil with petroleum hydrocarbons. Indian J Fund Appl Sci 2:300–305Google Scholar
  78. Philp JC, Whiteley AS, Ciric L, Bailey MJ (2005) Monitoring bioremediation. In: Atlas RM, Philp J (eds) Bioremediation: applied solution for a real-world environmental clean up. ASM Press, Washington D.C, pp 237–268CrossRefGoogle Scholar
  79. Pinto AJ, Raskin L (2012) PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS One 7:e43093CrossRefGoogle Scholar
  80. Pinyakong O, Habe H, Omori T (2003) The unique aromatic catabolic genes in sphingomonads degrading polycyclic aromatic hydrocarbons (PAHs). J Gen Appl Microbiol 49:1–19CrossRefGoogle Scholar
  81. Plohl K, Leskovesk H, Bricej M (2002) Biological biodegradation of motor oil in water. Acta Chim Slov 49:279–289Google Scholar
  82. Popp N, Schlomann M, Margit M (2006) Bacterial diversity in the active stage of a bioremediation system for mineral oil hydrocarbon-contaminated soils. Microbiology 152:3291–3304CrossRefGoogle Scholar
  83. Raeid MM, Al-Kharusi S, Al-Hinai M (2015) Effect of biostimulation, temperature and salinity on respiration activities and bacterial community composition in an oil polluted desert soil. Int Biodeterior Biodegrad 98:43–52CrossRefGoogle Scholar
  84. Rho M, Tang H, Ye Y (2010) FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acid Res 38:20–191CrossRefGoogle Scholar
  85. Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11(10):2477–2490CrossRefGoogle Scholar
  86. Salam LB, Obayori OS, Akashoro OS, Okogie GO (2011) Biodegradation of bonny light crude oil by bacteria isolated from contaminated soil. Int J Agric Biol 13:245–250Google Scholar
  87. Salam LB, Ilori MO, Amund OO et al (2014) Carbazole angular dioxygenation and mineralization by bacteria isolated from hydrocarbon-contaminated tropical African soil. Environ Sci Pollut Res 21:9311–9324CrossRefGoogle Scholar
  88. Salam LB, Obayori OS, Raji RA (2015) Biodegradation of used engine oil by a methylotrophic bacterium, Methylobacterium mesophilicum isolated from tropical hydrocarbon-contaminated soil. Petrol Sci Technol 33:186–119CrossRefGoogle Scholar
  89. Salam LB (2016) Metabolism of waste engine oil by Pseudomonas species. 3. Biotech 6:98Google Scholar
  90. 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 53:141–155CrossRefGoogle Scholar
  91. Sentchillo VSPA, Zehnder AJB, van der Meer JR (2000) Molecular diversity of plasmids bearing genes that encode toluene and xylene metabolism in Pseudomonas strains isolated from different contaminated sites in Belarus. Appl Environ Microbiol 66:2842–2852CrossRefGoogle Scholar
  92. Shah V, Zakrzewski M, Wibberg D, Eikmeyer D, Schluter A, Madamwar D (2013) Taxonomic profiling and metagenomic analysis of a microbial community from a habitat contaminated with industrial discharges. Microb Ecol 66:533–550CrossRefGoogle Scholar
  93. Sierra-Garcia IN, Alvarez JC, De Vansconcellos SP, de Souza AP, des Neto EU, Oliveira VM (2014) New hydrocarbon degradation pathways in the microbial metagenome from Brazilian petroleum reservoirs. PLoS One 9(2):e90087. doi: 10.1371/Journal.pone.0090087 CrossRefGoogle Scholar
  94. Singh V, Chauhan PK, Kanta R, Dhewa T, Kumar V (2010) Isolation and characterization of Pseudomonas resistant to heavy metals contaminants. Int J Pharm Sci Rev Res 3:164–167Google Scholar
  95. Smits TH, Witholt B, van Beilen JB (2003) Functional characterization of genes involved in alkane oxidation by Pseudomonas aeruginosa. Ant Van Leeu 84:193–200CrossRefGoogle Scholar
  96. Sophos NA, Vasiliou V (2003) Aldehyde dehydrogenase gene superfamily: the 2002 update. Chem Biol Interact 143–144:5–22CrossRefGoogle Scholar
  97. Spain A, Alm E (2003) Implications of microbial heavy metal tolerance in the environment. Rev Undergraduate Res 2:1–6Google Scholar
  98. Suenaga H, Koyama Y, Miyakoshi M et al (2009) Novel organization of aromatic degradation pathway genes in a microbial community as revealed by metagenomic analysis. ISME J 3:1335–1348CrossRefGoogle Scholar
  99. Suenaga H, Ohnuki T, Miyazaki K (2007) Functional screening of a metagenomic library for genes involved in microbial degradation of aromatic compounds. Environ Microbiol 9:2289–2297CrossRefGoogle Scholar
  100. Sutton NB, Maphosa F, Morillo JA et al (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79:619–630CrossRefGoogle Scholar
  101. Streit WR, Schmitz RA (2004) Metagenomics- key to the uncultured microbes. Curr Opin Microbiol 7:492–498CrossRefGoogle Scholar
  102. Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417CrossRefGoogle Scholar
  103. Talfournier F, Stines-Chaumeil C, Branlant G (2011) Methylmalonate semialdehyde dehydrogenase from Bacillus subtilis: substrate specificity and coenzyme a binding. J Biol Chem 286(25):21971–21981CrossRefGoogle Scholar
  104. Tatusov RL, Natale DA, Garkavtsev IV et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28CrossRefGoogle Scholar
  105. Top EM, Springael D (2003) The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol 14:262–269CrossRefGoogle Scholar
  106. Umechuruba CI (2005) Health impact assessment of mangrove vegetation in an oil spilled sitr at the Bodo West fields in Rivers State, Nigeria. J Appl Sci Environ Man 9:69–73Google Scholar
  107. Vaillancourt FH, Bolin JT, Eltis LD (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41:241–267CrossRefGoogle Scholar
  108. van Beilen JB, Panke S, Lucchini S, Franchini AG, Rothlisberger M, Witholt B (2001) Analysis of Pseudomonsas putida alkane degradation gene clusters and flanking insertion sequences: evolution and regulation of the alk-genes. Microbiol 147:1621–1630CrossRefGoogle Scholar
  109. Vasiliou V, Pappa A, Petersen DR (2000) Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem Biol Interact 129:1–19CrossRefGoogle Scholar
  110. Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73:1163–1172CrossRefGoogle Scholar
  111. Villadangos AF, Fu H-L, Gil JA, Messens J, Rosen BP, Meteos LM (2012) Efflux permease CgAcr3-1 of Corynebacterium glutamicum is an arsenite-specific antiporter. J Biol Chem 287(1):723–735CrossRefGoogle Scholar
  112. Vivas A, Moreno B, del Val C, Macci C, Masciandaro G, Benitez E (2008) Metabolic and bacterial diversity in soils historically contaminated by heavy metals and hydrocarbons. J Environ Monit 10:1287–1296CrossRefGoogle Scholar
  113. Wang W, Shao Z (2013) Enzymes and genes involved in aerobic alkane degradation. Frontiers Microbiol 4(116):1–7Google Scholar
  114. Wang L, Wang LFT, Liu H (2007) Treatment of engine oil polluted wastewater with mixed bacterial floral and kinetics of biodegradation. J Chongqing Univ 6:238–241Google Scholar
  115. Wu M, Dick WA, Li W, Chen L (2016) Bioaugmentation and biostimulation of hydrocarbon degradation and the microbial community in a petroleum-contaminated soil. Int Biodeter Biodegrad 107:158–164Google Scholar
  116. Yang S, Wen X, Jin H, Wu Q (2012) Pyrosequencing investigation into the bacterial community in permafrost soils along the China-Russia crude oil pipeline (CRCOP). PLoS One 7:e52730CrossRefGoogle Scholar
  117. Yang S, Wen X, Zhao L, Shi Y, Jin H (2014) Crude oil treatment leads to shift of bacterial communities in soils from the deep active layer and upper permafrost along the China-Russia crude oil pipeline route. PLoS One 9(5):e96552CrossRefGoogle Scholar
  118. Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PLoS One 7:e30058. doi: 10.1371/journal.pone.0030058 CrossRefGoogle Scholar
  119. Zhang YQ, Chen J, Liu HY, Zhang YQ, Li WJ, Yu L-Y (2011) Geodermatophilus ruber sp. nov., isolated from rhizosphere soil of a medicinal plant. Int J Syst Evol Microbiol 61(1):190–193CrossRefGoogle Scholar
  120. Zhou S, Zhang S, Lai D et al (2013) Biocatalytic characterization of a short-chain alcohol dehydrogenase with broad substrate specificity from thermophilic Carboxydothermus hydrogenoformans. Biotechnol Lett 35(3):359–336CrossRefGoogle Scholar
  121. Zhang DC, Mortelmaier C, Margesin R (2012) Characterization of the bacterial archaeal diversity in hydrocarbon-contaminated soil. Sci Total Environ 421-422:184–196CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Lateef B. Salam
    • 1
    Email author
  • Sunday O. Obayori
    • 2
  • Francisca O. Nwaokorie
    • 3
  • Aisha Suleiman
    • 1
  • Raheemat Mustapha
    • 1
  1. 1.Microbiology Unit, Department of Biological SciencesAl-Hikmah UniversityIlorinNigeria
  2. 2.Department of MicrobiologyLagos State UniversityOjoNigeria
  3. 3.Department of Medical Laboratory Science, College of MedicineUniversity of LagosAkokaNigeria

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