Advertisement

Microbial Communities in Hydrocarbon-Contaminated Desert Soils

  • Thirumahal Muthukrishnan
  • Raeid M. M. Abed
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Desert ecosystems are vulnerable to heavy crude oil spills during oil exploration and extraction processes. Oil-contaminated deserts exhibit harsh environmental conditions such as extreme temperatures, lack of water, nutrient deficiency, and the persistence of high concentrations of hydrocarbon compounds in soils. Over the past three decades, more attention has been directed to the study of oil-degrading microbial communities in oil-polluted desert ecosystems. In this chapter, current knowledge on hydrocarbon-degrading microbial communities in desert soils and their responses to bioremediation treatments as assessed using culture-based and molecular approaches has been reviewed. Diverse groups of bacteria and fungi have been detected in oil-polluted desert soils despite the severe environmental conditions. Bioremediation approaches including landfarming, phytoremediation, and the use of nutrients and vitamin mixtures have proven to be successful in the cleanup of oil-polluted desert soils. However, bioaugmentation approaches have not succeeded in most cases due to the inability of exogenous microorganisms to compete with indigenous microorganisms in desert soils. Further investigations are required to scale up bioremediation treatments and test their applicability in field conditions. More research should also be focused on the use of genomic and proteomic approaches to study the functional diversity and activities of microorganisms in oil-polluted desert soils.

References

  1. Abed RMM, Al Sabahi J, Al Maqrashi F, Al Habsi A, Al Hinai M (2014) Characterization of hydrocarbon degrading bacteria isolated from oil contaminated sediment in the Sultanate of Oman and evaluation of bioaugmentation and biostimulation approaches in microcosm experiments. Int Biodeterior Biodegrad 89:58–66CrossRefGoogle Scholar
  2. Abed RMM, Al-Kindi S, Al-Kharusi S (2015a) Diversity of bacterial communities along a petroleum contamination gradient in desert soils. Microb Ecol 69:95–105CrossRefPubMedGoogle Scholar
  3. Abed RMM, Al-Kharusi S, Al-Hinai M (2015b) 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
  4. Aislabie J, Foght J, Saul D (2000) Aromatic hydrocarbon-degrading bacteria from soil near Scott Base, Antarctica. Polar Biol 23:183–188CrossRefGoogle Scholar
  5. Aislabie J, Fraser R, Duncan S, Farrell RL (2001) Effects of oil spills on microbial heterotrophs in Antarctic soils. Polar Biol 24:308–313CrossRefGoogle Scholar
  6. Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10:171–179CrossRefPubMedGoogle Scholar
  7. Akbari A, Ghoshal S (2015) Effects of diurnal temperature variation on microbial community and petroleum hydrocarbon biodegradation in contaminated soils from a sub-Arctic site. Environ Microbiol 17:4916–4928CrossRefPubMedGoogle Scholar
  8. Al-Awadhi H, Al-Mailem D, Dashti N, Khanafer M, Radwan S (2012) Indigenous hydrocarbon-utilizing bacterioflora in oil-polluted habitats in Kuwait, two decades after the greatest man-made oil spill. Arch Microbiol 194:689–705CrossRefPubMedGoogle Scholar
  9. Ali N, Dashti N, Al-Mailem D, Eliyas M, Radwan S (2012) Indigenous soil bacteria with the combined potential for hydrocarbon consumption and heavy metal resistance. Environ Sci Pollut Res 19:812–820CrossRefGoogle Scholar
  10. Ali N, Dashti N, Salamah S, Sorkhoh N, Al-Awadhi H, Radwan S (2016a) Dynamics of bacterial populations during bench-scale bioremediation of oily seawater and desert soil bioaugmented with coastal microbial mats. Microb Biotechnol 9:157–171CrossRefPubMedPubMedCentralGoogle Scholar
  11. Ali N, Dashti N, Salamah S, Al-Awadhi H, Sorkhoh N, Radwan S (2016b) Autochthonous bioaugmentation with environmental samples rich in hydrocarbonoclastic bacteria for bench-scale bioremediation of oily seawater and desert soil. Environ Sci Pollut Res 23:8686–8698CrossRefGoogle Scholar
  12. Al-Kharusi S, Abed RMM, Dobretsov S (2016a) Changes in respiration activities and bacterial communities in a bioaugmented oil-polluted soil in response to the addition of acyl homoserine lactones. Int Biodeterior Biodegrad 107:165–173CrossRefGoogle Scholar
  13. Al-Kharusi S, Abed RMM, Dobretsov S (2016b) EDTA addition enhances bacterial respiration activities and hydrocarbon degradation in bioaugmented and non-bioaugmented oil-contaminated desert soils. Chemosphere 147:279–286CrossRefPubMedGoogle Scholar
  14. Al-Kindi S, Abed RMM (2016a) Comparing oil degradation efficiency and bacterial communities in contaminated soils subjected to biostimulation using different organic wastes. Water Air Soil Pollut 227:36CrossRefGoogle Scholar
  15. Al-Kindi S, Abed RMM (2016b) Effect of biostimulation using sewage sludge, soybean meal, and wheat straw on oil degradation and bacterial community composition in a contaminated desert soil. Front Microbiol 7:240CrossRefPubMedPubMedCentralGoogle Scholar
  16. Al-Mahruki A, Al Mueini R, Al-Mahrooqi Y, Al-Sabahi A, Roos GHP, Patzelt H (2006) Significantly enhanced landfarming performance through the use of saline water and weekly tilling. In: Proceedings of the SPE international conference on health and safety, and environment in oil and gas exploration and production, Abu Dhabi, SPE-98568-PPGoogle Scholar
  17. Al-Mailem DM, Kansour MK, Radwan SS (2015) Moderately thermophilic, hydrocarbonoclastic bacterial communities in Kuwaiti desert soil: enhanced activity via Ca2+ and dipicolinic acid amendment. Extremophiles 19:573–583CrossRefPubMedGoogle Scholar
  18. Al-Mueini R, Al-Dalali M, Al-Amri IS, Patzelt H (2007) Hydrocarbon degradation at high salinity by a novel extremely halophilic actinomycete. Environ Chem 4:5–7CrossRefGoogle Scholar
  19. Álvarez LM, Ruberto LA, Balbo AL, Mac Cormack WP (2017) Bioremediation of hydrocarbon-contaminated soils in cold regions: development of a pre-optimized biostimulation biopile-scale field assay in Antarctica. Sci Total Environ 590:194–203CrossRefGoogle Scholar
  20. Balba MT, Al-Daher R, Al-Awadhi N, Chino T, Tsuji H (1998) Bioremediation of oil-contaminated desert soil: the Kuwaiti experience. Environ Int 24:163–173CrossRefGoogle Scholar
  21. Barabás G, Sorkhoh NA, Fardoon F, Radwan SS (1995) n-Alkane-utilization by oligocarbophilic actinomycete strains from oil-polluted Kuwaiti desert soil. Actinomycetologica 9:13–18CrossRefGoogle Scholar
  22. Barabás G, Penyige A, Szabo I, Vargha G, Damjanovich S, Matko J, Szollosi J, Radwan SS, Matyus A, Hirano T (2000) Hydrocarbon uptake and utilization by Streptomyces strains. In: Wise DL, Trantolo DJ (eds) Remediation of hazardous wastes contaminated soils, 2nd edn. Marcel Dekker, New York, pp 291–309Google Scholar
  23. Barabás G, Vargha G, Szabó IM, Penyige A, Damjanovich S, Szöllösi J, Matkó J, Hirano T, Mátyus A, Szabó I (2001) n-Alkane uptake and utilisation by Streptomyces strains. Anton Leeuw 79:269–276CrossRefGoogle Scholar
  24. Baraniecki CA, Aislabie J, Foght JM (2002) Characterization of Sphingomonas sp. Ant 17, an aromatic hydrocarbon-degrading bacterium isolated from Antarctic soil. Microb Ecol 43:44–54CrossRefPubMedGoogle Scholar
  25. Bej AK, Saul D, Aislabie J (2000) Cold-tolerant alkane-degrading Rhodococcus species from Antarctica. Polar Biol 23:100–105CrossRefGoogle Scholar
  26. Bell TH, Yergeau E, Martineau C, Juck D, Whyte LG, Greer CW (2011) Identification of nitrogen-incorporating bacteria in petroleum-contaminated arctic soils by using [15N] DNA-based stable isotope probing and pyrosequencing. Appl Environ Microbiol 77:4163–4171CrossRefPubMedPubMedCentralGoogle Scholar
  27. Cho BN, Chino H, Tsuji H, Kunito T, Nagaoka K, Otsuka S, Yamashita K, Matsumoto S, Oyaizu H (1997a) Laboratory-scale bioremediation of oil-contaminated soil of Kuwait with soil amendment materials. Chemosphere 35:1599–1611CrossRefPubMedGoogle Scholar
  28. Cho BN, Chino H, Tsuji H, Kunito T, Makishima H, Uchida H, Matsumoto S, Oyaizu H (1997b) Analysis of oil components and hydrocarbon-utilizing microorganisms during laboratory-scale bioremediation of oil-contaminated soil of Kuwait. Chemosphere 35:1613–1621CrossRefPubMedGoogle Scholar
  29. Dashti N, Al-Awadhi H, Khanafer M, Abdelghany S, Radwan S (2008) Potential of hexadecane-utilizing soil-microorganisms for growth on hexadecanol, hexadecanal and hexadecanoic acid as sole sources of carbon and energy. Chemosphere 70:475–479CrossRefPubMedGoogle Scholar
  30. Dashti N, Khanafer M, El-Nemr I, Sorkhoh N, Ali N, Radwan S (2009) The potential of oil-utilizing bacterial consortia associated with legume root nodules for cleaning oily soils. Chemosphere 74:1354–1359CrossRefPubMedGoogle Scholar
  31. Dashti N, Ali N, Eliyas M, Khanafer M, Sorkhoh NA, Radwan SS (2015) Most hydrocarbonoclastic bacteria in the total environment are diazotrophic, which highlights their value in the bioremediation of hydrocarbon contaminants. Microbes Environ 30:70–75CrossRefPubMedPubMedCentralGoogle Scholar
  32. Delille D, Coulon F, Pelletier E (2004a) Biostimulation of natural microbial assemblages in oil-amended vegetated and desert sub-Antarctic soils. Microb Ecol 47:407–415CrossRefPubMedGoogle Scholar
  33. Delille D, Coulon F, Pelletier E (2004b) Effects of temperature warming during a bioremediation study of natural and nutrient-amended hydrocarbon-contaminated sub-Antarctic soils. Cold Reg Sci Technol 40:61–70CrossRefGoogle Scholar
  34. Dias RL, Ruberto L, Hernández E, Vázquez SC, Balbo AL, Del Panno MT, Mac Cormack WP (2012) Bioremediation of an aged diesel oil-contaminated Antarctic soil: evaluation of the “on site” biostimulation strategy using different nutrient sources. Int Biodeterior Biodegrad 75: 96–103CrossRefGoogle Scholar
  35. Eckford R, Cook FD, Saul D, Aislabie J, Foght J (2002) Free-living heterotrophic nitrogen-fixing bacteria isolated from fuel-contaminated Antarctic soils. Appl Environ Microbiol 68:5181–5185CrossRefPubMedPubMedCentralGoogle Scholar
  36. El-Nawawy AS, Al-Daher R, Yateem A (1999) Plant–soil interaction during bioremediation of oil contaminated soil. In: Kostecki P, Behbehani M (eds) Assessment and remediation of oil contaminated soils. New Age International, Kuwait, pp 218–224Google Scholar
  37. Embar K, Forgacs C, Sivan A (2006) The role of indigenous bacterial and fungal soil populations in the biodegradation of crude oil in a desert soil. Biodegradation 17:369–377CrossRefPubMedGoogle Scholar
  38. Eriksson M, Dalhammar G, Mohn WW (2002) Bacterial growth and biofilm production on pyrene. FEMS Microbiol Ecol 40:21–27CrossRefPubMedGoogle Scholar
  39. Farrell RL, Rhodes PL, Aislabie J (2003) Toluene-degrading Antarctic Pseudomonas strains from fuel-contaminated soil. Biochem Biophys Res Commun 312:235–240CrossRefPubMedGoogle Scholar
  40. Gerhardt P, Marquis RE (1989) Spore thermoresistance mechanisms. In: Smith I, Slepecky RA, Setlow P (eds) Regulation of prokaryotic development. American Society for Microbiology, Washington, DC, pp 43–63Google Scholar
  41. Godoy-Faúndez A, Antizar-Ladislao B, Reyes-Bozo L, Camaño A, Sáez-Navarrete C (2008) Bioremediation of contaminated mixtures of desert mining soil and sawdust with fuel oil by aerated in-vessel composting in the Atacama Region (Chile). J Hazard Mater 151:649–657CrossRefPubMedGoogle Scholar
  42. Hassan N, Rafiq M, Hayat M, Shah AA, Hasan F (2016) Psychrophilic and psychrotrophic fungi: a comprehensive review. Rev Environ Sci Biotechnol 15:147–172CrossRefGoogle Scholar
  43. Hughes KA, Bridge P, Clark MS (2007) Tolerance of Antarctic soil fungi to hydrocarbons. Sci Total Environ 372:539–548CrossRefPubMedGoogle Scholar
  44. Kaplan CW, Kitts CL (2004) Bacterial succession in a petroleum land treatment unit. Appl Environ Microbiol 70:1777–1786CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kerry E (1990) Microorganisms colonizing plants and soil subjected to different degrees of human activity, including petroleum contamination, in the Vestfold Hills and MacRobertson Land, Antarctica. Polar Biol 10:423–430Google Scholar
  46. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315PubMedPubMedCentralGoogle Scholar
  47. Mac Cormack WP, Fraile ER (1997) Characterization of a hydrocarbon degrading psychrotrophic Antarctic bacterium. Antarct Sci 9:150–155Google Scholar
  48. Mahmoud HM, Suleman P, Sorkhoh NA, Salamah S, Radwan SS (2010) The potential of established turf cover for cleaning oily desert soil using rhizosphere technology. Int J Phytorem 13:156–167CrossRefGoogle Scholar
  49. Makut MD, Ishaya P (2010) Bacterial species associated with soils contaminated with used petroleum products in Keffi town, Nigeria. Afr J Microbiol Res 4:1698–1702Google Scholar
  50. Margesin R, Schinner F (2001) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Microbiol Biotechnol 56:650–663CrossRefPubMedPubMedCentralGoogle Scholar
  51. Master ER, Mohn WW (1998) Psychrotolerant bacteria isolated from Arctic soil that degrade polychlorinated biphenyls at low temperatures. Appl Environ Microbiol 64:4823–4829PubMedPubMedCentralGoogle Scholar
  52. McKinnon M, Vine P (1991) Tides of war. IMMEL, LondonGoogle Scholar
  53. Mohamed ME, Al-Dousary M, Hamzah RY, Fuchs G (2006) Isolation and characterization of indigenous thermophilic bacteria active in natural attenuation of bio-hazardous petrochemical pollutants. Int Biodeterior Biodegrad 58:213–223CrossRefGoogle Scholar
  54. Noble IR, Gitay H (1996) Deserts in a changing climate: impacts. In: Watson RT, Zinyowera MC, Moss RH, Dokken DJ (eds) Climate change: impact, adaptation and migration of climate change: scientific–technical analysis. Cambridge University Press, New York, pp 159–165Google Scholar
  55. Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:25–51CrossRefGoogle Scholar
  56. Obuekwe CO, Al-Jadi ZK, Al-Saleh ES (2009) Hydrocarbon degradation in relation to cell-surface hydrophobicity among bacterial hydrocarbon degraders from petroleum-contaminated Kuwait desert environment. Int Biodeterior Biodegrad 63:273–279CrossRefGoogle Scholar
  57. Panicker G, Aislabie J, Saul D, Bej AK (2002) Cold tolerance of Pseudomonas sp. 30-3 isolated from oil-contaminated soil, Antarctica. Polar Biol 25:5–11CrossRefGoogle Scholar
  58. Pruthi V, Cameotra SS (1997) Production and properties of a biosurfactant synthesized by Arthrobacter protophormiae, an Antarctic strain. World J Microbiol Biotechnol 13:137–139CrossRefGoogle Scholar
  59. Radwan SS (1990) Gulf oil spill. Nature 350:456CrossRefGoogle Scholar
  60. Radwan S (1998) Hydrocarbon uptake by Streptomyces. FEMS Microbiol Lett 169:87–94CrossRefPubMedGoogle Scholar
  61. Radwan S (2008) Microbiology of oil-contaminated desert soils and coastal areas in the Arabian Gulf region. In: Patrice D, Chandra SN (eds) Microbiology of extreme soils, 13th edn. Springer, Berlin/Heidelberg, pp 275–298CrossRefGoogle Scholar
  62. Radwan S (2009) Phytoremediation for oily desert soils. In: Singh A, Kuhad RC, Ward OP (eds) Advances in applied bioremediation. Springer, Berlin/Heidelberg, pp 279–298CrossRefGoogle Scholar
  63. Radwan SS, Al-Muteirie AS (2001) Vitamin requirements of hydrocarbon-utilizing soil bacteria. Microbiol Res 155:301–307CrossRefPubMedGoogle Scholar
  64. Radwan SS, Sorkhoh NA (1997) A feasibility study on seeding as a bioremediation practice for the oily Kuwaiti desert. J Appl Microbiol 83:353–358CrossRefGoogle Scholar
  65. Radwan SS, Sorkhoh NA, Al-Hasan RH (1995a) Self-cleaning and bioremediation potential of the Arabian Gulf. In: Cheremisinoff P (ed) Encyclopedia of environmental control technology, vol 9. Gulf, Houston, pp 901–924Google Scholar
  66. Radwan S, Sorkhoh N, Israa EN (1995b) Oil biodegradation around roots. Nature 376:302–302CrossRefPubMedGoogle Scholar
  67. Radwan SS, Sorkhoh NA, Fardoun F, Al-Hasan RH (1995c) Soil management enhancing hydrocarbon biodegradation in the polluted Kuwaiti desert. Appl Microbiol Biotechnol 44:265–270CrossRefPubMedGoogle Scholar
  68. Radwan SS, Al-Awadhi H, El-Nemr IM (2000) Cropping as a phytoremediation practice for oily desert soil with reference to crop safety as food. Int J Phytorem 2:383–396CrossRefGoogle Scholar
  69. Radwan SS, Al-Mailem DM, Kansour MK (2017) Calcium (II) – and dipicolinic acid mediated-biostimulation of oil-bioremediation under multiple stresses by heat, oil and heavy metals. Sci Rep 7:9534CrossRefPubMedPubMedCentralGoogle Scholar
  70. Ravelet C, Krivobok S, Sage L, Steiman R (2000) Biodegradation of pyrene by sediment fungi. Chemosphere 40:557–563CrossRefPubMedGoogle Scholar
  71. Reyes-Bozo L, Antizar-Lalislao B, Sáez-Navarrete C, Godoy-Faúndeza A (2010) Bioremediation of TOCs present in fuel-contaminated desert mining soil and sawdust in the Atacama region (Chile). In: Proceedings of the annual international conference on soils, sediments, water and energy, vol 13, article 4. http://scholarworks.umass.edu/soilsproceedings/vol13/iss1/4
  72. Ruberto LA, Vazquez S, Lobalbo A, Mac Cormack WP (2005) Psychrotolerant hydrocarbon-degrading Rhodococcus strains isolated from polluted Antarctic soils. Antarct Sci 17:47–56CrossRefGoogle Scholar
  73. Saadoun I, Mohammad MJ, Hameed KM, Shawaqfah MA (2008) Microbial populations of crude oil spill polluted soils at the Jordan–Iraq desert (the Badia region). Braz J Microbiol 39:453–456CrossRefPubMedPubMedCentralGoogle Scholar
  74. Sanscartier D, Zeeb B, Koch I, Reimer K (2009) Bioremediation of diesel-contaminated soil by heated and humidified biopile system in cold climates. Cold Reg Sci Technol 55:167–173CrossRefGoogle Scholar
  75. 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 53:141–155CrossRefPubMedGoogle Scholar
  76. Setlow B, Atluri S, Kitchel R, Koziol-Dube K, Setlow P (2006) Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective α/β-type small acid-soluble proteins. J Bacteriol 188:3740–3747CrossRefPubMedPubMedCentralGoogle Scholar
  77. Sorkhoh NA, Ghannoum MA, Ibrahim AS, Stretton RJ, Radwan SS (1990) Crude oil and hydrocarbon-degrading strains of Rhodococcus rhodochrous isolated from soil and marine environments in Kuwait. Environ Pollut 65:1–17CrossRefPubMedGoogle Scholar
  78. Sorkhoh NA, Ibrahim AS, Ghannoum MA, Radwan SS (1993) High-temperature hydrocarbon degradation by Bacillus stearothermophilus from oil-polluted Kuwaiti desert. Appl Microbiol Biotechnol 39:123–126CrossRefGoogle Scholar
  79. Sorkhoh NA, Al-Hasan RH, Khanafer M, Radwan SS (1995) Establishment of oil-degrading bacteria associated with cyanobacteria in oil-polluted soil. J Appl Microbiol 78:194–199Google Scholar
  80. Sorkhoh NA, Ali N, Dashti N, Al-Mailem DM, Al-Awadhi H, Eliyas M, Radwan SS (2010a) Soil bacteria with the combined potential for oil utilization, nitrogen fixation, and mercury resistance. Int Biodeterior Biodegrad 64:226–231CrossRefGoogle Scholar
  81. Sorkhoh NA, Ali N, Salamah S, Eliyas M, Khanafer M, Radwan SS (2010b) Enrichment of rhizospheres of crop plants raised in oily sand with hydrocarbon-utilizing bacteria capable of hydrocarbon consumption in nitrogen free media. Int Biodeterior Biodegrad 64:659–664CrossRefGoogle Scholar
  82. Subhash Y, Yoon DE, Lee SS (2017) Skermanella mucosa sp. nov., isolated from crude oil contaminated soil. Anton Leeuw 13:1–8Google Scholar
  83. Sutton NB, Maphosa F, Morillo JA, Al-Soud WA, Langenhoff AA, Grotenhuis T, Rijnaarts HH, Smidt H (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79:619–630CrossRefPubMedPubMedCentralGoogle Scholar
  84. Thomassin-Lacroix EJ, Yu Z, Eriksson M, Reimer KJ, Mohn WW (2001) DNA-based and culture-based characterization of a hydrocarbon-degrading consortium enriched from Arctic soil. Can J Microbiol 47:1107–1115CrossRefPubMedGoogle Scholar
  85. Thomassin-Lacroix E, Eriksson M, Reimer K, Mohn W (2002) Biostimulation and bioaugmentation for on-site treatment of weathered diesel fuel in Arctic soil. Appl Microbiol Biotechnol 59:551–556CrossRefPubMedGoogle Scholar
  86. Thompson KT, Crocker FH, Fredrickson HL (2005) Mineralization of the cyclic nitramine explosive hexahydro-1, 3, 5-trinitro-1, 3, 5-triazine by Gordonia and Williamsia spp. Appl Environ Microbiol 71:8265–8272CrossRefPubMedPubMedCentralGoogle Scholar
  87. Torsvik V, Øvreås L (2008) Microbial diversity, life strategies, and adaptation to life in extreme soils. In: Patrice D, Chandra SN (eds) Microbiology of extreme soils, 13th edn. Springer, Berlin/Heidelberg, pp 15–43CrossRefGoogle Scholar
  88. Whyte LG, Bourbonniere L, Greer CW (1997) Biodegradation of petroleum hydrocarbons by psychrotrophic Pseudomonas strains possessing both alkane (alk) and naphthalene (nah) catabolic pathways. Appl Environ Microbiol 63:3719–3723PubMedPubMedCentralGoogle Scholar
  89. Whyte LG, Slagman SJ, Pietrantonio F, Bourbonniere L, Koval SF, Lawrence JR, Inniss WE, Greer CW (1999) Physiological adaptations involved in alkane assimilation at a low temperature by Rhodococcus sp. strain Q15. Appl Environ Microbiol 65:2961–2968PubMedPubMedCentralGoogle Scholar
  90. Whyte LG, Smits THM, Labbè D, Witholt B, Greer CW, Van Beilen JB (2002a) Gene cloning and characterization of multiple alkane hydroxilase systems in Rhodococcus strains Q15 and NRRL B16531. Appl Environ Microbiol 68:5933–5942CrossRefPubMedPubMedCentralGoogle Scholar
  91. Whyte LG, Schultz A, Van Beilen JB, Luz AP, Pellizari V, Labbè D, Greer CW (2002b) Prevalence of alkane monooxygenase genes in Arctic and Antarctic hydrocarbon-contaminated and pristine soils. FEMS Microbiol Ecol 41:141–150PubMedGoogle Scholar
  92. 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:e96552CrossRefPubMedPubMedCentralGoogle Scholar
  93. Yateem A (2013) Rhizoremediation of oil-contaminated sites: a perspective on the Gulf War environmental catastrophe on the State of Kuwait. Environ Sci Pollut Res 20:100–107CrossRefGoogle Scholar
  94. Yateem A, Balba MT, El-Nawawy AS, Al-Awadhi N (2000) Plants-associated microflora and the remediation of oil-contaminated soil. Int J Phytorem 2:183–191CrossRefGoogle Scholar
  95. Yateem A, Balba MT, Al-Shayji Y, Al-Awadhi N (2002) Isolation and characterization of biosurfactant-producing bacteria from oil-contaminated soil. Soil Sediment Contam 11:41–55CrossRefGoogle Scholar
  96. Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PLoS One 7:e30058CrossRefPubMedPubMedCentralGoogle Scholar
  97. Yu Z, Stewart GR, Mohn WW (2000) Apparent contradiction: psychrotolerant bacteria from hydrocarbon-contaminated arctic tundra soils that degrade diterpenoids synthesized by trees. Appl Environ Microbiol 66:5148–5154CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.College of Science, Biology DepartmentSultan Qaboos UniversityMuscatSultanate of Oman

Personalised recommendations