Advertisement

Bioremediation of Contaminated Environments Using Rhodococcus

  • Maria S. KuyukinaEmail author
  • Irena B. Ivshina
Chapter
Part of the Microbiology Monographs book series (MICROMONO, volume 16)

Abstract

Environmental pollution with anthropogenic organic compounds is the global problem of our planet. Bioremediation has a great potential to effectively restore polluted environments by using biodegradative activities of microorganisms. The genus Rhodococcus is a promising group of bacteria suitable for biodegradation of recalcitrant contaminants, such as petroleum hydrocarbons, chlorinated, nitrogenated, and other complex organics. Rhodococcus species are ubiquitous in pristine and contaminated environments, survive under harsh environmental conditions, compete successfully in complex bacterial populations, and therefore could be efficiently used in bioremediation applications. Some success in bioremediation of contaminated soils, waters, and air has been achieved using rhodococci either as bioaugmentation agents or members of indigenous microbial communities stimulated by nutrient and oxygen amendments. Laboratory and field-scale studies on Rhodococcus application in cleanup technologies are reviewed relating to in situ subsurface and groundwater remediation, on-site treatments of contaminated soils, sludges, wastewaters, and gaseous emissions.

Notes

Acknowledgments

This research was funded by the Ministry of Science and Higher Education of the Russian Federation (State Task Registration No. 01201353247 for IEGM) and the Russian Science Foundation grant 18-14-00140 for PSU.

References

  1. Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10:171–179PubMedPubMedCentralCrossRefGoogle Scholar
  2. Al-Awadhi H, Al-Hasan RH, Sorkhoh NA, Salamah S, Radwan SS (2003) Establishing oil-degrading biofilms on gravel particles and glass plates. Int Biodeterior Biodegrad 51:181–185CrossRefGoogle Scholar
  3. Aldric J-M, Thonart P (2008) Performance evaluation of a water/silicone oil two-phase partitioning bioreactor using Rhodococcus erythropolis T902.1 to remove volatile organic compounds from gaseous effluents. J Chem Technol Biotechnol 83:1401–1408CrossRefGoogle Scholar
  4. Alexander M (1999) Biodegradation and bioremediation, vol 2. Academic Press, LondonGoogle Scholar
  5. An X, Cheng Y, Huang M, Sun Y, Wang H, Chen X, Wang J, Li D, Li C (2018) Treating organic cyanide-containing groundwater by immobilization of a nitrile-degrading bacterium with a biofilm-forming bacterium using fluidized bed reactors. Environ Pollut 237:908–916PubMedCrossRefPubMedCentralGoogle Scholar
  6. Aoshima H, Hirase T, Tada T, Ichimura N, Kato H, Nagata Y, Myoenzono T, Tagauchi M, Takuzumi T, Aoki T, Makino S, Hagita K, Ishiwata H (2007) Safety evaluation of a heavy oil-degrading bacterium Rhodococcus erythropolis C2. J Toxicol Sci 32:69–78PubMedCrossRefPubMedCentralGoogle Scholar
  7. Baxter J, Cummings SP (2006) The impact of bioaugmentation on metal cyanide degradation and soil bacteria community structure. Biodegradation 17:207–217PubMedCrossRefPubMedCentralGoogle Scholar
  8. Baxter J, Garton NJ, Cummings SP (2006) The impact of acrylonitrile and bioaugmentation on the biodegradation activity and bacterial community structure of a topsoil. Folia Microbiol 51:591–597CrossRefGoogle Scholar
  9. Bej AK, Saul D, Aislabie J (2000) Cold-tolerant alkane-degrading Rhodococcus species from Antarctica. Polar Biol 23:100–105CrossRefGoogle Scholar
  10. Bell KS, Philp JC, Aw DWJ, Christofi N (1998) The genus Rhodococcus. A review. J Appl Microbiol 85:195–210PubMedPubMedCentralCrossRefGoogle Scholar
  11. Beškoski VP, Miletić S, Ilić M, Gojgić-Cvijović G, Papić P, Marić N, Šolević-Knudsen T, Jovančićević BS, Nakano T, Vrvić MM (2017) Biodegradation of isoprenoids, steranes, terpanes and phenanthrenes during in situ bioremediation of petroleum contaminated groundwater. Clean Soil Air Water 45:1600023.  https://doi.org/10.1002/clen.201600023CrossRefGoogle Scholar
  12. Besse P, Combourieu B, Boyse G, Sancelme M, de Wever H, Delort A-M (2001) Long-range 1H-15N heteronuclear shift correlation at natural abundance: a tool to study benzothiazole biodegradation by two Rhodococcus strains. Appl Environ Microbiol 67:1412–1417PubMedPubMedCentralCrossRefGoogle Scholar
  13. Borin S, Marzorati M, Brusetti L, Zilli M, Cherif H, Hassen A, Converti A, Sorlini C, Daffonchio D (2006) Microbial succession in a compost-packed biofilter treating benzene-contaminated air. Biodegradation 17:79–89CrossRefGoogle Scholar
  14. Borràs E, Caminal G, Sarrà M, Novotný C (2010) Effect of soil bacteria on the ability of polycyclic aromatic hydrocarbons (PAHs) removal by Trametes versicolor and Irpex lacteus from contaminated soil. Soil Biol Biochem 42:2087–2093CrossRefGoogle Scholar
  15. Cappelletti M, Pinelli D, Fedi S, Zannoni D, Frascari D (2018) Aerobic co-metabolism of 1,1,2,2-tetrachloroethane by Rhodococcus aetherivorans TPA grown on propane: kinetic study and bioreactor configuration analysis. J Chem Technol Biotechnol 93:155–165CrossRefGoogle Scholar
  16. Cavalca L, Colombo M, Larcher S, Gigliotti C, Collina E, Andreoni V (2002) Survival and naphthalene-degrading activity of Rhodococcus sp. strain 1BN in soil microcosms. J Appl Microbiol 92:1058–1065PubMedCrossRefPubMedCentralGoogle Scholar
  17. Christofi N, Ivshina IB, Kuyukina MS, Philp JC (1998) Biological treatment of crude oil contaminated soil in Russia. In: Lerner DN, London NRG (eds) Contaminated land and groundwater: future directions, vol 14. Geological Society Engineering Geology Publications, London, pp 45–51Google Scholar
  18. Coffey L, Owens E, Tambling K, O’Neill D, O’Connor L, O’Reilly C (2010) Real-time PCR detection of Fe-type nitrile hydratase genes from environmental isolates suggests horizontal gene transfer between multiple genera. Antonie Van Leeuwenhoek 98:455–463PubMedCrossRefPubMedCentralGoogle Scholar
  19. Coleman NV, Nelson DR, Duxbury T (1998) Aerobic biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) as a nitrogen source by a Rhodococcus sp., strain DN22. Soil Biol Biochem 30:1159–1167CrossRefGoogle Scholar
  20. Colquhoun JA, Heald SC, Tamaoka LLJ, Kato C, Horikoshi K, Bull AT (1998) Taxonomy and biotransformation activities of some deep-sea actinomycetes. Extremophiles 2:269–277PubMedPubMedCentralGoogle Scholar
  21. Daghio M, Tatangelo V, Franzetti A, Gandolfi I, Papacchini M, Careghini A, Sezenna E, Saponaro S, Bestetti G (2015) Hydrocarbon degrading microbial communities in bench scale aerobic biobarriers for gasoline contaminated groundwater treatment. Chemosphere 130:34–39.  https://doi.org/10.1016/j.chemosphere.2015.02.022CrossRefPubMedPubMedCentralGoogle Scholar
  22. Daye KJ, Groff JC, Kirpekar AC, Mazumder R (2003) High efficiency degradation of tetrahydrofuran (THF) using a membrane bioreactor: identification of THF-degrading cultures of Pseudonocardia sp. strain M1 and Rhodococcus ruber isolate M2. J Ind Microbiol Biotechnol 30:705–714PubMedCrossRefPubMedCentralGoogle Scholar
  23. Dean-Ross D, Moody JD, Freeman JP, Doerge DR, Cerniglia CE (2001) Metabolism of anthracene by a Rhodococcus species. FEMS Microbiol Lett 204:205–211PubMedCrossRefPubMedCentralGoogle Scholar
  24. Dejonghe W, Boon N, Seghers D, Top EM, Verstraete W (2001) Bioaugmentation of soils by increasing microbial richness: missing links. Environ Microbiol 3:649–657PubMedCrossRefPubMedCentralGoogle Scholar
  25. De-qing S, Jian Z, Zhao-long G, Jian D, Tian-li W, Murygina V, Kalyuzhnyi S (2007) Bioremediation of oil sludge in Shengli oilfield. Water Air Soil Pollut 185:177–184CrossRefGoogle Scholar
  26. Di Lorenzo A, Varcamonti M, Parascandola P, Vignola R, Bernardi A, Sacceddu P, Sisto R, de Alteriis E (2005) Characterization and performance of a toluene-degrading biofilm developed on pumice stones. Microb Cell Factories 4:4CrossRefGoogle Scholar
  27. Dobslaw D, Engesser K-H (2018) Biodegradation of gaseous emissions of 2-chlorotoluene by strains of Rhodococcus sp. in polyurethane foam packed biotrickling filters. Sci Total Environ 639:1491–1500PubMedCrossRefPubMedCentralGoogle Scholar
  28. Dogan OB, Onal-Ulusoy B, Bozoglu F, Sagdicoglu-Celep AG, Cekmecelioglu D (2017) Detoxification of groundnut cake naturally contaminated with aflatoxin B1 using Rhodococcus erythropolis in shake flask bioreactors. Waste Biomass Valoriz 8:721–731CrossRefGoogle Scholar
  29. Elo S, Maunuksela L, Salkinoja-Salonen M, Smolander A, Haahtela K (2000) Humus bacteria of Norway spruce stands: plant growth promoting properties and birch, red fescue and alder colonizing capacity. FEMS Microbiol Ecol 31:143–152PubMedCrossRefGoogle Scholar
  30. Etkin DS (2001) Analysis of oil spill trends in the United States and worldwide. Proceeding of the International Oil Spill Conference. American Petroleum Institute, Washington, pp 1291–1300CrossRefGoogle Scholar
  31. Fahy A, McGenity TJ, Timmis KN, Ball AS (2006) Heterogeneous aerobic benzene-degrading communities in oxygen-depleted groundwaters. FEMS Microbiol Ecol 58:260–270PubMedCrossRefGoogle Scholar
  32. Fahy A, Ball AS, Lethbridge G, McGenity TJ, Timmis KN (2008a) High benzene concentrations can favour Gram-positive bacteria in groundwaters from a contaminated aquifer. FEMS Microbiol Ecol 65:526–533PubMedCrossRefPubMedCentralGoogle Scholar
  33. Fahy A, Ball AS, Lethbridge G, Timmis KN, McGenity TJ (2008b) Isolation of alkali-tolerant benzene-degrading bacteria from a contaminated aquifer. Lett Appl Microbiol 47:60–66PubMedCrossRefGoogle Scholar
  34. Fava F, Bertin L, Fedi S, Zannoni D (2003) Methyl-β-cyclodextrin-enhanced solubilization and aerobic biodegradation of polychlorinated biphenyls in two aged-contaminated soils. Biotechnol Bioeng 81:381–390PubMedCrossRefPubMedCentralGoogle Scholar
  35. Fayolle-Guichard F, Durand J, Cheucle M, Rosell M, Michelland RJ, Tracol J-P, Le Roux F, Grundman G, Atteia O, Richnow HH, Dumestre A, Benoit Y (2012) Study of an aquifer contaminated by ethyl tert-butyl ether (ETBE): site characterization and on-site bioremediation. J Hazard Mater 201–202:236–243PubMedCrossRefPubMedCentralGoogle Scholar
  36. Federici E, Pepi M, Esposito A, Scargetta S, Fidati L, Gasperini S, Cenci G, Altieri R (2011) Two-phase olive mill waste composting: community dynamics and functional role of the resident microbiota. Bioresour Technol 102:10965–10972PubMedCrossRefPubMedCentralGoogle Scholar
  37. Fuller ME, Hatzinger PB, Condee CW, Andaya C, Vainberg S, Michalsen MM, Crocker FH, Indest KJ, Jung CM, Eaton H, Istok JD (2015) Laboratory evaluation of bioaugmentation for aerobic treatment of RDX in groundwater. Biodegradation 26:77–89.  https://doi.org/10.1007/s10532-014-9717-yCrossRefPubMedPubMedCentralGoogle Scholar
  38. Gakhar L, Malik ZA, Allen CCR, Lipscomb DA, Larkin MJ, Ramaswamy S (2005) Structure and increased thermostability of Rhodococcus sp. naphthalene 1,2-dioxygenase. J Bacteriol 187:7222–7231PubMedPubMedCentralCrossRefGoogle Scholar
  39. Genovese M, Denaro R, Cappello S, Di Marco G, La Spada G, Giuliano L, Genovese L, Yakimov MM (2008) Bioremediation of benzene, toluene, ethylbenzene, xylenes-contaminated soil: a biopile pilot experiment. J Appl Microbiol 105:1694–1702PubMedCrossRefGoogle Scholar
  40. Hamamura N, Olson SH, Ward DM, Inskeep WP (2006) Microbial population dynamics associated with crude-oil biodegradation in diverse soils. Appl Environ Microbiol 72:6316–6324PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hasan HA, Abdullah SRS, Al-Attabi AWN, Nash DAH, Anuar N, Rahman NA, Titah HS (2016) Removal of ibuprofen, ketoprofen, COD and nitrogen compounds from pharmaceutical wastewater using aerobic suspension-sequencing batch reactor (ASSBR). Sep Purif Technol 157:215–221CrossRefGoogle Scholar
  42. Hatzinger PB, Condee C, McClay KR, Togna AP (2011) Aerobic treatment of N-nitrosodimethylamine in a propane-fed membrane bioreactor. Water Res 45:254–262PubMedCrossRefGoogle Scholar
  43. Hatzinger PB, Lewis C, Webster TS (2017) Biological treatment of N-nitrosodimethylamine (NDMA) and N-nitrodimethylamine (NTDMA) in a field-scale fluidized bed bioreactor. Water Res 126:361–371PubMedCrossRefGoogle Scholar
  44. Hendrickx B, Dejonghe W, Boenne W, Brennerova M, Cernik M, Lederer T, Bucheli-Witschel M, Bastiaens L, Verstraete W, Top EM, Diels L, Springa D (2005) Dynamics of an oligotrophic bacterial aquifer community during contact with a groundwater plume contaminated with benzene, toluene, ethylbenzene, and xylenes: an in situ mesocosm study. Appl Environ Microbiol 71:3815–3825PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hidalgo A, Jaureguibeitia A, Prieto MB, Rodríguez-Fernández C, Serra JL, Llama MJ (2002a) Biological treatment of phenolic industrial wastewaters by Rhodococcus erythropolis UPV-1. Enzyme Microb Technol 31:221–226CrossRefGoogle Scholar
  46. Hidalgo A, Lopategi A, Prieto M, Serra JL, Llama MJ (2002b) Formaldehyde removal in synthetic and industrial wastewater by Rhodococcus erythropolis UPV-1. Appl Microbiol Biotechnol 58:260–263PubMedCrossRefGoogle Scholar
  47. Home Pages of Culture Collections in the World (2018) World federation for culture collections. http://www.wfcc.info/index.php/collections/. Cited 20 Jul 2018
  48. Homklin S, Kee Ong S, Limpiyakorn T (2012) Degradation of 17α-methyltestosterone by Rhodococcus sp. and Nocardioides sp. isolated from a masculinizing pond of Nile tilapia fry. J Hazard Mater 221–222:35–44PubMedCrossRefGoogle Scholar
  49. Hong SH, Hae LP, Ko U-R, Jae JY, Cho K-S (2007) Bioremediation of oil-contaminated soil using an oil-degrading rhizobacterium Rhodococcus sp. 412 and Zea mays. Korean J Microbiol Biotechnol 35:150–157Google Scholar
  50. Hongming L, Xu L, Zhaojian G, Fan Y, Dingbin C, Jianchun Z, Jianhong X, Shunpeng L, Qing H (2015) Isolation of an aryloxyphenoxy propanoate (AOPP) herbicide-degrading strain Rhodococcus ruber JPL-2 and the cloning of a novel carboxylesterase gene (feh). Braz J Microbiol 46:425–432PubMedPubMedCentralCrossRefGoogle Scholar
  51. Ito K, Kawashima F, Takagi K, Kataoka R, Kotake M, Kiyota H, Yamazaki K, Sakakibara F, Okada S (2016) Isolation of endosulfan sulfate-degrading Rhodococcus koreensis strain S1-1 from endosulfan contaminated soil and identification of a novel metabolite, endosulfan diol monosulfate. Biochem Biophys Res Commun 473:1094–1099PubMedCrossRefPubMedCentralGoogle Scholar
  52. Ivshina IB, Oborin AA, Nesterenko OA, Kasumova SA (1981) Bacteria of the Rhodococcus genus from the ground water of oil-bearing deposits in the Perm region near the Urals. Microbiology (Moscow) 50:709–717Google Scholar
  53. Ivshina IB, Kamenskikh TN, Liapunov YE (1994) IEGM catalogue of strains of regional specialized collection of alkanotrophic microorganisms. Nauka, MoscowGoogle Scholar
  54. Ivshina IB, Berdichevskaya MV, Zvereva LV, Rybalka LV, Elovikova EA (1995) Phenotypic characterization of alkanotrophic rhodococci from various ecosystems. Microbiology (Moscow) 64:507–513Google Scholar
  55. Ivshina IB, Peshkur TA, Korobov VP (2002) Effective uptake of cesium ions by Rhodococcus cells. Microbiology (Moscow) 71:357–361CrossRefGoogle Scholar
  56. Ivshina IB, Kuyukina MS, Kostina LV (2013) Adaptive mechanisms of nonspecific resistance to heavy metal ions in alkanotrophic actinobacteria. Russ J Ecol 44:123–130CrossRefGoogle Scholar
  57. Ivshina IB, Kuyukina MS, Krivoruchko AV, Elkin AA, Makarov SO, Cunningham CJ, Peshkur TA, Atlas RM, Philp JC (2015a) Oil spill problems and sustainable response strategies through new technologies. Environ Sci Process Impacts 17:1201–1219PubMedCrossRefPubMedCentralGoogle Scholar
  58. Ivshina IB, Mukhutdinova AN, Tyumina HA, Suzina NE, El’-Registan GI, Mulyukin AL (2015b) Drotaverine hydrochloride degradation using cyst-like dormant cells of Rhodococcus ruber. Curr Microbiol 70:307–314PubMedCrossRefPubMedCentralGoogle Scholar
  59. Ivshina I, Kostina L, Krivoruchko A, Kuyukina M, Peshkur T, Anderson P, Cunningham C (2016) Removal of polycyclic aromatic hydrocarbons in soil spiked with model mixtures of petroleum hydrocarbons and heterocycles using biosurfactants from Rhodococcus ruber IEGM 231. J Hazard Mater 312:8–17PubMedCrossRefPubMedCentralGoogle Scholar
  60. Ivshina IB, Kuyukina MS, Krivoruchko AV (2017) Hydrocarbon-oxidizing bacteria and their potential in eco-biotechnology and bioremediation. In: Kurtböke I (ed) Microbial resources: from functional existence in nature to industrial applications. Elsevier, Amsterdam, pp 121–148CrossRefGoogle Scholar
  61. Jiménez N, Viñas M, Bayona JM, Albaiges J, Solanas AM (2007) The Prestige oil spill: bacterial community dynamics during a field biostimulation assay. Appl Microbiol Biotechnol 77:935–945PubMedCrossRefPubMedCentralGoogle Scholar
  62. Joshi T, Iyengar L, Singh K, Garg S (2008) Isolation, identification and application of novel bacterial consortium TJ-1 for the decolourization of structurally different azo dyes. Bioresour Technol 99:7115–7121PubMedCrossRefPubMedCentralGoogle Scholar
  63. Juneson C, Ward OP, Singh A (2001) Biodegradation of bis(2-ethylhexyl)phthalate in a soil slurry-sequencing batch reactor. Proc Biochem 37:305–313CrossRefGoogle Scholar
  64. Juteau P, Larocque R, Rho D, LeDuy A (1999) Analysis of the relative abundance of different types of bacteria capable of toluene degradation in a compost biofilter. Appl Microbiol Biotechnol 52:863–868PubMedCrossRefPubMedCentralGoogle Scholar
  65. Katsivela E, Bonse D, Krüger A, Strömpl C, Livingston C, Wittich R-M (1999) An extractive membrane biofilm reactor for degradation of 1,3-dichloropropene in industrial waste water. Appl Microbiol Biotechnol 52:853–862PubMedCrossRefPubMedCentralGoogle Scholar
  66. Kim J-D, Lee C-G (2007) Microbial degradation of polycyclic aromatic hydrocarbons in soil by bacterium-fungus co-cultures. Biotech Bioproc Eng 12:410–416CrossRefGoogle Scholar
  67. Kim D, Chae JC, Zylstra GJ, Kim YS, Kim SK, Nam MH, Kim YM, Kim E (2004) Identification of a novel dioxygenase involved in metabolism of o-xylene, toluene, and ethylbenzene by Rhodococcus sp. strain DK17. Appl Environ Microbiol 70:7086–7092PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kimbara K, Hayakawa T, Shimura M (1998) Remediating PCB wastes using microorganisms. Jpn Railway Transp Rev 17:17–20Google Scholar
  69. Kitagawa W, Tamura T (2008a) A quinoline antibiotic from Rhodococcus erythropolis JCM 6824. J Antibiot 61:680–682PubMedCrossRefPubMedCentralGoogle Scholar
  70. Kitagawa W, Tamura T (2008b) Three types of antibiotics produced from Rhodococcus erythropolis strains. Microbes Environ 23:167–171PubMedCrossRefPubMedCentralGoogle Scholar
  71. Kitamoto D, Isoda H, Nakahara T (2002) Functions and potential applications of glycolipid biosurfactants—from energy-saving materials to gene delivery carriers. J Biosci Bioeng 94:187–201PubMedCrossRefPubMedCentralGoogle Scholar
  72. Kitova AE, Kuvichkina TN, Arinbasarova AY, Reshetilov AN (2004) Degradation of 2,4-dinitrophenol by free and immobilized cells of Rhodococcus erythropolis HL PM-1. Appl Biochem Microbiol 40:258–261CrossRefGoogle Scholar
  73. Koronelli TV, Komarova TI, Il’inskii VV, Kuz’min YI, Kirsanov NB, Yanenko AS (1997) Introduction of bacteria of the genus Rhodococcus into oil-contaminated tundra soils. Appl Biochem Microbiol 33:172–175Google Scholar
  74. Kuyukina MS, Ivshina IB, Ritchkova MI, Philp JC, Cunningham JC, Christofi N (2003) Bioremediation of crude oil-contaminated soil using slurry-phase biological treatment and land farming techniques. Soil Sediment Contam 12:85–99CrossRefGoogle Scholar
  75. Kuyukina MS, Ivshina IB, Makarov SO, Litvinenko LV, Cunningham CJ, Philp JC (2005) Effect of biosurfactants on crude oil desorption and mobilization in a soil system. Environ Int 31:155–161PubMedCrossRefPubMedCentralGoogle Scholar
  76. Kuyukina MS, Ivshina IB, Gein SV, Baeva TA, Chereshnev VA (2007) In vitro immunomodulating activity of biosurfactant glycolipid complex from Rhodococcus ruber. Bull Exp Biol Med 144:326–330PubMedCrossRefPubMedCentralGoogle Scholar
  77. Kuyukina MS, Ivshina IB, Serebrennikova MK, Krivorutchko AV, Podorozhko EA, Ivanov RV, Lozinsky VI (2009) Petroleum-contaminated water treatment in a fluidized-bed bioreactor with immobilized Rhodococcus cells. Int Biodeter Biodegr 63:427–432CrossRefGoogle Scholar
  78. Kuyukina MS, Ivshina IB, Kamenskikh TN, Bulicheva MV, Stukova GI (2013) Survival of cryogel-immobilized Rhodococcus cells in crude oil-contaminated soil and their impact on biodegradation efficiency. Int Biodeter Biodegr 84:118–125CrossRefGoogle Scholar
  79. Kuyukina MS, Ivshina IB, Serebrennikova MK, Krivoruchko AV, Korshunova IO, Peshkur TA, Cunningham CJ (2017) Oilfield wastewater biotreatment in a fluidized-bed bioreactor using co-immobilized Rhodococcus cultures. J Environ Chem Eng 5:1252–1260CrossRefGoogle Scholar
  80. Labbé 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 59:466–475PubMedCrossRefPubMedCentralGoogle Scholar
  81. Lang S, Philp JC (1998) Surface-active lipids in rhodococci. Antonie Van Leeuwenhoek 74:59–70PubMedCrossRefPubMedCentralGoogle Scholar
  82. Larkin MJ, Kulakov LA, Allen CCR (2005) Biodegradation and Rhodococcus—masters of catabolic versatility. Curr Opin Biotechnol 16:282–290PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lee E-H, Cho K-S (2008) Characterization of cyclohexane and hexane degradation by Rhodococcus sp. EC1. Chemosphere 71:1738–1744PubMedCrossRefPubMedCentralGoogle Scholar
  84. Lin T-C, Pan P-T, Cheng S-S (2010) Ex situ bioremediation of oil-contaminated soil. J Hazard Mater 176:27–34PubMedCrossRefPubMedCentralGoogle Scholar
  85. López ME, Rene ER, Malhautier L, Rocher J, Bayle S, Veiga MC, Kennes C (2013) One-stage biotrickling filter for the removal of a mixture of volatile pollutants from air: performance and microbial community analysis. Bioresour Technol 138:245–252PubMedCrossRefPubMedCentralGoogle Scholar
  86. Luepromchai E, Singer AC, Yang C-H, Crowley DE (2002) Interactions of earthworms with indigenous and bioaugmented PCB-degrading bacteria. FEMS Microbiol Ecol 41:191–197PubMedCrossRefPubMedCentralGoogle Scholar
  87. Luz AP, Pellizari VH, Whyte LG, Greer CW (2004) A survey of indigenous microbial hydrocarbon degradation genes in soils from Antarctica and Brazil. Can J Microbiol 50:323–333PubMedPubMedCentralCrossRefGoogle Scholar
  88. Maqbool T, Khan SJ, Waheed H, Lee C-H, Hashmi I, Iqbal H (2015) Membrane biofouling retardation and improved sludge characteristics using quorum quenching bacteria in submerged membrane bioreactor. J Membr Sci 483:75–83CrossRefGoogle Scholar
  89. Margesin R, Labbé D, Schinner F, Greer CW, Whyte LG (2003) Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Appl Environ Microbiol 69:3085–3092PubMedPubMedCentralCrossRefGoogle Scholar
  90. Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177PubMedPubMedCentralCrossRefGoogle Scholar
  91. Masák J, Čejková A, Jirků V, Kotrba D, Hron P, Siglová M (2004) Colonization of surfaces by phenolic compounds utilizing microorganisms. Environ Int 31:197–200CrossRefGoogle Scholar
  92. Masy T, Bertrand C, Xavier P-M, Vreuls C, Wilmot A, Cludts M, Renard P, Mawet P, Smets S, Dethy B, Thonart P, Jacques P, Hiligsmann S (2016a) Stable biofilms of Rhodococcus erythropolis T902.1 in draining pavement structures for runoff water decontamination. Int Biodeter Biodegr 112:108–118CrossRefGoogle Scholar
  93. Masy T, Caterina D, Tromme O, Lavigne B, Thonart P, Hiligsmann S, Nguyen F (2016b) Electrical resistivity tomography to monitor enhanced biodegradation of hydrocarbons with Rhodococcus erythropolis T902.1 at a pilot scale. J Contam Hydrol 184:1–13PubMedCrossRefPubMedCentralGoogle Scholar
  94. Mergaert J, Verhelst A, Cnockaert MC, Tan T-L, Swings J (2001) Characterization of facultative oligotrophic bacteria from polar seas by analysis of their fatty acids and 16S rDNA sequences. Syst Appl Microbiol 24:98–107PubMedCrossRefPubMedCentralGoogle Scholar
  95. Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70:202–213PubMedPubMedCentralCrossRefGoogle Scholar
  96. Murygina V, Arinbasarov M, Kalyuzhnyi S (2000) Bioremediation of oil polluted aquatic systems and soils with novel preparation ‘Rhoder’. Biodegradation 11(6):385–389PubMedCrossRefGoogle Scholar
  97. Murygina VP, Markarova MY, Kalyuzhnyi SV (2005) Application of biopreparation Rhoder for remediation of oil polluted polar marshy wetlands in Komi Republic. Environ Int 31:163–166PubMedCrossRefPubMedCentralGoogle Scholar
  98. Nagy I, Schoofs G, Compernolle F, Proost P, Vanderleyden J, de Mot R (1995) Degradation of the thiocarbamate herbicide EPTC (s-ethyldipropylcarbamothioate) and biosafening by Rhodococcus sp. strain NI86/21 involve an inducible cytochrome P-450 system and aldehyde dehydrogenase. J Biotechnol 177:676–687Google Scholar
  99. Nie Y, Chi CQ, Fang H, Liang JL, Lu SL, Lai GL, Tang YQ, Wu XL (2014) Diverse alkane hydroxylase genes in microorganisms and environments. Sci Rep 4:4968.  https://doi.org/10.1038/srep04968CrossRefPubMedPubMedCentralGoogle Scholar
  100. Nwankwoala AU, Egiebor NO, Nyavor K (2001) Enhanced biodegradation of methylhydrazine and hydrazine contaminated NASA wastewater in fixed-film bioreactor. Biodegradation 12:1–10PubMedCrossRefPubMedCentralGoogle Scholar
  101. Ohhata N, Yoshida N, Egami H, Katsuragi T, Tani Y, Takagi H (2007) An extremely oligotrophic bacterium, Rhodococcus erythropolis N9T-4, isolated from crude oil. J Biotechnol 189:6824–6831Google Scholar
  102. Pei X, Wang J, Guo W, Miao J, Wang A (2017) Efficient biodegradation of dihalogenated benzonitrile herbicides by recombinant Escherichia coli harboring nitrile hydratase-amidase pathway. Biochem Eng J 125:88–96CrossRefGoogle Scholar
  103. Peressutti SR, Alvarez HM, Pucci OH (2003) Dynamics of hydrocarbon-degrading bacteriocenosis of an experimental oil pollution in Patagonian soil. Int Biodeter Biodegr 52:21–30CrossRefGoogle Scholar
  104. Petrić I, Hršak D, Fingler S, Vončina E, Ćetković H, Kolar AB, Kolić NU (2007) Enrichment and characterization of PCB-degrading bacteria as potential seed cultures for bioremediation of contaminated soil. Food Technol Biotechnol 45:11–20Google Scholar
  105. Pieper DH, Reineke W (2000) Engineering bacteria for bioremediation. Curr Opin Biotechnol 11:262–270PubMedCrossRefPubMedCentralGoogle Scholar
  106. Podorozhko EA, Lozinsky VI, Ivshina IB, Kuyukina MS, Krivorutchko AV, Philp JC, Cunningham CJ (2008) Hydrophobised sawdust as a carrier for immobilisation of the hydrocarbon-oxidizing bacterium Rhodococcus ruber. Bioresour Technol 99:2001–2008PubMedCrossRefPubMedCentralGoogle Scholar
  107. Poelarends GJ, Zandstra M, Bosma T, Kulakov LA, Larkin MJ, Marchesi JR, Weightman AJ, Janssen DB (2000) Haloalkane-utilizing Rhodococcus strains isolated from geographically distinct locations possess a highly conserved gene cluster encoding haloalkane catabolism. J Bacteriol 5:2725–2731CrossRefGoogle Scholar
  108. Priestley JT, Coleman NV, Duxbury T (2006) Growth rate and nutrient limitation affect the transport of Rhodococcus sp. strain DN22 through sand. Biodegradation 17:571–576PubMedCrossRefPubMedCentralGoogle Scholar
  109. Prieto MB, Hidalgo A, Rodríguez-Fernández C, Serra JL, Llama MJ (2002a) Biodegradation of phenol in synthetic and industrial wastewater by Rhodococcus erythropolis UPV-1 immobilized in an air-stirred reactor with clarifier. Appl Microbiol Biotechnol 58:853–859PubMedCrossRefPubMedCentralGoogle Scholar
  110. Prieto MB, Hidalgo A, Serra JL, Llama MJ (2002b) Degradation of phenol by Rhodococcus erythropolis UPV-1 immobilized on Biolite® in a packed-bed reactor. J Biotechnol 97:1–11CrossRefGoogle Scholar
  111. Ramos C, Amorim CL, Mesquita DP, Ferreira EC, Carrera J, Castro PML (2017) Simultaneous partial nitrification and 2-fluorophenol biodegradation with aerobic granular biomass: reactor performance and microbial communities. Bioresour Technol 238:232–240PubMedCrossRefPubMedCentralGoogle Scholar
  112. Ringelberg DB, Talley JW, Perkins EJ, Tucker SG, Luthy RG, Bouwer EJ, Fredrickson HL (2001) Succession of phenotypic, genotypic, and metabolic community characteristics during in vitro bioslurry treatment of polycyclic aromatic hydrocarbon-contaminated sediments. Appl Environ Microbiol 67:1542–1550PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rodrigues JLM, Kachel CA, Aiello MR, Quensen JF, Maltseva OV, Tsoi TV, Tiedje JM (2006) Degradation of Aroclor 1242 dechlorination products in sediments by Burkholderia xenovorans LB400(ohb) and Rhodococcus sp. strain RHA1(fcb). Appl Environ Microbiol 72:2476–2482PubMedPubMedCentralCrossRefGoogle Scholar
  114. Ruberto LAM, Vazquez S, Lobalbo A, Mac Cormack WP (2005) Psychrotolerant hydrocarbon-degrading Rhodococcus strains isolated from polluted Antarctic soils. Antarct Sci 17:47–56CrossRefGoogle Scholar
  115. Ryu HW, Yang HJ, Youn-J A, Kyung-Suk C (2006) Isolation and characterization of psychrotrophic and halotolerant Rhodococcus sp. YHLT-2. J Microbiol Biotechnol 16:605–612Google Scholar
  116. Safonova E, Kvitko KV, Iankevitch MI, Surgko LF, Afti IA, Reisser W (2004) Biotreatment of industrial wastewater by selected algal-bacterial consortia. Eng Life Sci 4:347–353CrossRefGoogle Scholar
  117. Salanitro JP, Spinnler GE, Maner PM, Tharpe DL, Pickle DW, Wisniewski HL, Johnson PC, Bruce C (2001) In situ bioremediation of MTBE using biobarriers of single or mixed cultures. In: Leeson A, Alleman BC, Alvarez PJ, Magar VS (eds) Bioaugmentation, biobarriers and biogeochemistry. Battelle Press, Columbus, OH, pp 1–7Google Scholar
  118. Serebrennikova MK, Golovina EE, Kuyukina MS, Ivshina IB (2017) A consortium of immobilized rhodococci for oilfield wastewater treatment in a column bioreactor. Appl Biochem Microbiol 53:435–440CrossRefGoogle Scholar
  119. Seth-Smith HMB, Rosser SJ, Basran A, Travis ER, Dabbs ER, Nicklin S, Bruce NC (2002) Cloning, sequencing, and characterization of the hexahydro-1,3,5-trinitro-1,3,5-triazine degradation gene cluster from Rhodococcus rhodochrous. Appl Environ Microbiol 68(10):4764–4771PubMedPubMedCentralCrossRefGoogle Scholar
  120. Shagol CC, Krishnamoorthy R, Kim K, Sundaram S, Sa T (2014) Arsenic-tolerant plant-growth-promoting bacteria isolated from arsenic-polluted soils in South Korea. Environ Sci Pollut Res 21:9356–9365CrossRefGoogle Scholar
  121. Sharma SL, Pant A (2000) Biodegradation and conversion of alkanes and crude oil by a marine Rhodococcus sp. Biodegradation 11:289–294PubMedCrossRefPubMedCentralGoogle Scholar
  122. Shen J, He R, Yu H, Wang L, Zhang J, Sun X, Li J, Han W, Xu L (2009a) Biodegradation of 2,4,6-trinitrophenol (picric acid) in a biological aerated filter (BAF). Bioresour Technol 100:1922–1930PubMedCrossRefPubMedCentralGoogle Scholar
  123. Shen J, Zhang J, Zuo Y, Wang L, Sun X, Li J, Han W, He R (2009b) Biodegradation of 2,4,6-trinitrophenol by Rhodococcus sp. isolated from a picric acid-contaminated soil. J Hazard Mater 163:1199–1206PubMedCrossRefPubMedCentralGoogle Scholar
  124. Sidorov DG, Borzenkov IA, Ibatullin RR, Milekhina EI, Khramov IT, Belyaev SS, Ivanov MV (1997) A field experiment on decontamination of oil-polluted soil employing hydrocarbon-oxidizing microorganisms. Appl Biochem Microbiol 33:441–445Google Scholar
  125. Sidorov DG, Borzenkov IA, Milekhina EI, Belyaev SS, Ivanov MV (1998) Microbial destruction of fuel oil in soil induced by the biological preparation Devoroil. Appl Biochem Microbiol 34:255–260Google Scholar
  126. Sinha RK, Krishnan KP, Hatha AA, Rahiman M, Thresyamma DD, Kerkar S (2017) Diversity of retrievable heterotrophic bacteria in Kongsfjorden, an Arctic fjord. Braz J Microbiol 48:51–61PubMedCrossRefPubMedCentralGoogle Scholar
  127. 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 65:1–17PubMedCrossRefPubMedCentralGoogle Scholar
  128. Sorkhoh NA, Al-Hasan RH, Khanafer M, Radwan SS (1995) Establishment of oil-degrading bacteria associated with cyanobacteria in oil-polluted soil. J Appl Bacteriol 78:194–199PubMedCrossRefPubMedCentralGoogle Scholar
  129. Sun G-D, Xu Y, Jin J-H, Zhong Z-P, Liu Y, Luo M, Liu Z-P (2012) Pilot scale ex-situ bioremediation of heavily PAHs-contaminated soil by indigenous microorganisms and bioaugmentation by a PAHs-degrading and bioemulsifier-producing strain. J Hazard Mater 233–234:72–78PubMedCrossRefPubMedCentralGoogle Scholar
  130. Taheri HE, Hatamipour MS, Emtiazi G, Beheshti M (2008) Bioremediation of DSO contaminated soil. Proc Saf Environ Protect 86:208–212CrossRefGoogle Scholar
  131. Tajima T, Hayashida N, Matsumura R, Omura A, Nakashimada Y, Kato J (2012) Isolation and characterization of tetrahydrofuran-degrading Rhodococcus aetherivorans strain M8. Process Biochem 47:1665–1669CrossRefGoogle Scholar
  132. Taki H, Syutsubo K, Mattison RG, Harayama S (2004) Biodegradation of o-xylene in soil using bioaugmentation technology. Proceedings of the Second International Conference on Remediation of Contaminated Sediments, pp 279–283Google Scholar
  133. Taki H, Syutsubo K, Mattison RG, Harayama S (2007) Identification and characterization of o-xylene-degrading Rhodococcus spp. which were dominant species in the remediation of o-xylene-contaminated soils. Biodegradation 18:17–26PubMedCrossRefPubMedCentralGoogle Scholar
  134. Táncsics A, Benedek T, Szoboszlay S, Veres PG, Farkas M, Máthé I, Márialigeti K, Kukolya J, Lányi S, Kriszt B (2015) The detection and phylogenetic analysis of the alkane1-monooxygenase gene of members of the genus Rhodococcus. Syst Appl Microbiol 38:1–7PubMedCrossRefPubMedCentralGoogle Scholar
  135. Tartakovsky B, Michotte A, Cadieux J-CA, Lau PCK, Hawari J, Guiot SR (2001) Degradation of Aroclor 1242 in a single-stage coupled anaerobic/aerobic bioreactor. Water Res 35:4323–4330PubMedCrossRefPubMedCentralGoogle Scholar
  136. Thomassin-Lacroix EJM, Eriksson M, Reimer KJ, Mohn WW (2002) Biostimulation and bioaugmentation for on-site treatment of weathered diesel fuel in Arctic soil. Appl Microbiol Biotechnol 59:551–556PubMedCrossRefPubMedCentralGoogle Scholar
  137. Travkin V, Baskunov BP, Golovlev EL, Boersma MG, Boeren S, Vervoort J, van Berkel WJH, Rietjens MCM, Golovleva LA (2002) Reductive deamination as a new step in the anaerobic microbial degradation of halogenated anilines. FEMS Microbiol Lett 209:307–312PubMedCrossRefPubMedCentralGoogle Scholar
  138. Tresse O, Lorrain M-J, Rho D (2002) Population dynamics of free-floating and attached bacteria in a styrene-degrading biotrickling filter analyzed by denaturing gradient gel electrophoresis. Appl Microbiol Biotechnol 59:585–590PubMedCrossRefPubMedCentralGoogle Scholar
  139. Uroz S, D’Angelo-Picard C, Carlier A, Elasri M, Sicot C, Petit A, Oger P, Faure D, Dessaux Y (2003) Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria. Microbiology 149:1981–1989PubMedCrossRefPubMedCentralGoogle Scholar
  140. US EPA 2017 Superfund remedy report, 15th edn. EPA-542-R-17-001. Office of Superfund Remediation and Technology Innovation (OSRTI)Google Scholar
  141. Van der Geize R, Dijkhuizen L (2004) Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr Opin Microbiol 7:255–261PubMedPubMedCentralCrossRefGoogle Scholar
  142. Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549PubMedPubMedCentralCrossRefGoogle Scholar
  143. Van Veen JA, van Overbeek LS, van Elsas JD (1997) Fate and activity of microorganisms introduced into soil. Microbiol Mol Biol Rev 61:121–135PubMedPubMedCentralGoogle Scholar
  144. Vergara-Fernández A, Yánez D, Morales P, Scott F, Aroca G, Diaz-Robles L, Moreno-Casas P (2018) Biofiltration of benzo[α]pyrene, toluene and formaldehyde in air by a consortium of Rhodococcus erythropolis and Fusarium solani: effect of inlet loads, gas flow and temperature. Chem Eng J 332:702–710CrossRefGoogle Scholar
  145. Vinage P, von Rohr R (2003) Biological waste gas treatment with a modified rotating biological contactor. I. Control of biofilm growth and long-term performance. Bioprocess Biosyst Eng 26:69–74PubMedCrossRefPubMedCentralGoogle Scholar
  146. Vogt C, Alfreidera A, Lorbeerb H, Hoffmanna D, Wuenschea L, Babel W (2004) Bioremediation of chlorobenzene-contaminated ground water in an in situ reactor mediated by hydrogen peroxide. J Contam Hydrol 68:121–141PubMedCrossRefPubMedCentralGoogle Scholar
  147. Wagner-Döbler I, Bennasar A, Vancanneyt M, Strömpl C, Brümmer I, Eichner C, Grammel I, Moore ERB (1998) Microcosm enrichment of biphenyl-degrading microbial communities from soils and sediments. Appl Environ Microbiol 64:3014–3022PubMedPubMedCentralGoogle Scholar
  148. Warhurst AM, Fewson CA (1994) Biotransformations catalyzed by the genus Rhodococcus. Crit Rev Biotechnol 14:29–73CrossRefGoogle Scholar
  149. Watanabe K, Hamamura N (2003) Molecular and physiological approaches to understanding the ecology of pollutant degradation. Curr Opin Biotechnol 14:289–295PubMedCrossRefPubMedCentralGoogle Scholar
  150. Wattiau P (2002) Microbial aspects in bioremediation of soils polluted by polyaromatic hydrocarbons. In: Agathos SN, Reineke W (eds) Biotechnol for the environment: strategy and fundamentals. Kluwer Academic Publishers, Netherlands, pp 69–89CrossRefGoogle Scholar
  151. Weerasekara NA, Choo K-H, Lee C-H (2016) Biofouling control: bacterial quorum quenching versus chlorination in membrane bioreactors. Water Res 103:293–301PubMedCrossRefGoogle Scholar
  152. Weidhaas JL, Schroeder ED, Chang DPY (2007) An aerobic sequencing batch reactor for 2,4,6-trinitrophenol (picric acid) biodegradation. Biotechnol Bioeng 97:1408–1414PubMedCrossRefGoogle Scholar
  153. Whyte LG, Hawari J, Zhou E, Bourbonniere L, Inniss WE, Greer CW (1998) Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic Rhodococcus sp. Appl Environ Microbiol 64:2578–2584PubMedPubMedCentralGoogle Scholar
  154. Whyte LG, Slagman SJ, Pietrantonio F, Bourbonniere L, Koval SF, Lawrence JR, Innis WE, Greer SW (1999) Physiological adaptations involved in alkane assimilation at a low temperature by Rhodococcus sp. strain Q15. Appl Environ Microbiol 65:2961–2968PubMedPubMedCentralGoogle Scholar
  155. Whyte LG, Goalen B, Hawari J, Labbé D, Greer CW, Nahir M (2001) Bioremediation treatability assessment of hydrocarbon-contaminated soils from Eureka, Nunavut. Cold Reg Sci Technol 32:121–132CrossRefGoogle Scholar
  156. Whyte LG, Schultz A, van Beilen JB, Luz AP, Pellizari V, Labbé D, Greer CW (2002a) Prevalence of alkane monooxygenase genes in Arctic and Antarctic hydrocarbon-contaminated and pristine. FEMS Microb Ecol 41:141–150Google Scholar
  157. Whyte LG, Smits TH, Labbé D, Witholt B, Greer CW, van Beilen JB (2002b) Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus strains Q15 and NRRL B-16531. Appl Environ Microbiol 68:5933–5942PubMedPubMedCentralCrossRefGoogle Scholar
  158. Xu P, Yu B, Li FL, Cai XF, Ma CQ (2006) Microbial degradation of sulfur, nitrogen and oxygen heterocycles. Trends Microbiol 14:397–404CrossRefGoogle Scholar
  159. Yaacob NS, Mohamad R, Ahmad SA, Abdullah H, Ibrahim AL, Ariff AB (2016) The influence of different modes of bioreactor operation on the efficiency of phenol degradation by Rhodococcus UKMP-5M. Rend Lincei 27:749–760.  https://doi.org/10.1007/s12210-016-0567-xCrossRefGoogle Scholar
  160. Yang X, Xie F, Zhang G, Shi Y, Qian S (2008) Purification, characterization, and substrate specificity of two 2,3-dihydroxybiphenyl 1,2-dioxygenase from Rhodococcus sp. R04, showing their distinct stability at various temperature. Biochimie 90:1530–1538PubMedCrossRefPubMedCentralGoogle Scholar
  161. Zagustina NA, Misharina TA, Veprizky AA, Zhukov VG, Ruzhitsky AO, Terenina MB, Krikunova NI, Kulikova AK, Popov VO (2012) Elimination of volatile compounds of leaf tobacco from air emissions using biofiltration. Appl Biochem Microbiol 48:385–395CrossRefGoogle Scholar
  162. Zhang K, Liu Y, Chen Q, Luo H, Zhu Z, Chen W, Chen J, Mo Y (2018) Biochemical pathways and enhanced degradation of di-n-octyl phthalate (DOP) in sequencing batch reactor (SBR) by Arthrobacter sp. SLG-4 and Rhodococcus sp. SLG-6 isolated from activated sludge. Biodegradation 29(2):171–185.  https://doi.org/10.1007/s10532-018-9822-4CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of Ecology and Genetics of Microorganisms, Perm Scientific Centre of the Ural Branch of the Russian Academy of SciencesPerm State UniversityPermRussia

Personalised recommendations