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Anaerobic Microbial Degradation of Polycyclic Aromatic Hydrocarbons: A Comprehensive Review

  • Kartik Dhar
  • Suresh R. Subashchandrabose
  • Kadiyala Venkateswarlu
  • Kannan Krishnan
  • Mallavarapu MegharajEmail author
Chapter
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 251)

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are a class of hazardous organic contaminants that are widely distributed in nature, and many of them are potentially toxic to humans and other living organisms. Biodegradation is the major route of detoxification and removal of PAHs from the environment. Aerobic biodegradation of PAHs has been the subject of extensive research; however, reports on anaerobic biodegradation of PAHs are so far limited. Microbial degradation of PAHs under anaerobic conditions is difficult because of the slow growth rate of anaerobes and low energy yield in the metabolic processes. Despite the limitations, some anaerobic bacteria degrade PAHs under nitrate-reducing, sulfate-reducing, iron-reducing, and methanogenic conditions. Anaerobic biodegradation, though relatively slow, is a significant process of natural attenuation of PAHs from the impacted anoxic environments such as sediments, subsurface soils, and aquifers. This review is intended to provide comprehensive details on microbial degradation of PAHs under various reducing conditions, to describe the degradation mechanisms, and to identify the areas that should receive due attention in further investigations.

Keywords

2-Naphthoic acid Aerobic biodegradation Anaerobic biodegradation Anoxia Aromatic ring reduction Benzo(a)pyrene Biodegradation Bioremediation Fate of PAHs Genetics Iron-reducing bacteria  Mechanism of anaerobic biodegradation Metabolite profiling Methanogenic bacteria Microbial degradation Naphthalene Naphthalene carboxylase Nitrate-reducing bacteria PAH sources  Pathways of biodegradation Phenanthrene Polycyclic aromatic hydrocarbons Pyrene Sulfate-reducing bacteria Thermodynamics 

Abbreviations

ΔG°′

Standard Gibbs free energy change

1,2,3,4-THNA

1,2,3,4-Tetrahydro-2-naphthoic acid

1-MN

1-Methylnaphthalene

1-NA

1-Naphthoic acid

2-DMNA

2-Dimethylnaphthalene

2-MN

2-Methylnaphthalene

2-NA

2-Naphthoic acid

5,6,7,8-THNA

5,6,7,8-Tetrahydro-2-naphthoic acid

ADP

Adenosine diphosphate

ATP

Adenosine triphosphate

BaP

Benzo(a)pyrene

Bcr

Benzoyl-CoA reductase

BESA

Bromoethane sulfonic acid

Bns

Beta-oxidation of naphthyl-2-methylsuccinate

Bss

Benzylsuccinate synthase

BTEX

Benzene, toluene, ethylbenzene, and xylene

CoA

Coenzyme A

DO

Dissolved oxygen

E0′

Standard reduction potential

FBR

Fluidized bed reactor

GC

Gas chromatography

H2O2

Hydrogen peroxide

HH-2-NA

Hexahydro-2-naphthoic acid

HMW

High molecular weight

kDa

Kilodalton

LC

Liquid chromatography

LC-ESI-MS-MS

Liquid chromatography electrospray ionization tandem mass spectrometry

LiP

Lignin peroxidase

LMW

Low molecular weight

logKOW

Octanol-water partition coefficient

MGP

Manufactured gas plant sites

MNA

Methylnaphthoic acid

MnP

Manganese-dependent peroxidase

MS

Mass spectrometry

Ncr

Naphthoyl-CoA reductase

NMeS

Naphthyl-2-methylenesuccinic acid

Nms

2-Napthylmethylsuccinate synthase

NMS

Naphthyl-2-methylsuccinic acid

NRB

Nitrate-reducing bacteria

OYE

Old yellow enzyme

PAHs

Polycyclic aromatic hydrocarbons

POP

Persistent organic pollutants

PpcA

Phenylphosphate carboxylase

Q-TOF-MS

Quadrupole time-of-flight mass spectrometry

rRNA

Ribosomal RNA

SOM

Soil organic matter

SRB

Sulfate-reducing bacteria

TCA

Tricarboxylic acid

TEA

Terminal electron acceptor

THNA

Tetrahydronaphthoic acid

TOC

Total organic carbon

T-RFLP

Terminal restriction fragment length polymorphism

UbiD

3-Polyprenyl-4-hydroxybenzoate decarboxylase

US EPA

United States Environmental Protection Agency

Notes

Acknowledgment

Kartik Dhar is grateful to the University of Newcastle for UNIPRS and UNRS central scholarship and to the University of Chittagong, Chittagong 4331, Bangladesh, for granting study leave.

Conflict of Interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. Abdel-Shafy HI, Mansour MSM (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25:107–123Google Scholar
  2. Abu Laban N, Selesi D, Rattei T, Tischler P, Meckenstock RU (2010) Identification of enzymes involved in anaerobic benzene degradation by a strictly anaerobic iron-reducing enrichment culture. Environ Microbiol 12:2783–2796Google Scholar
  3. Achten C, Hofmann T (2009) Native polycyclic aromatic hydrocarbons (PAH) in coals – a hardly recognized source of environmental contamination. Sci Total Environ 407:2461–2473Google Scholar
  4. Acosta-González A, Marqués S (2016) Bacterial diversity in oil-polluted marine coastal sediments. Curr Opin Biotechnol 38:24–32Google Scholar
  5. Agarry SE, Owabor CN (2011) Anaerobic bioremediation of marine sediment artificially contaminated with anthracene and naphthalene. Environ Technol 32:1375–1381Google Scholar
  6. Aitken CM, Jones DM, Larter S (2004) Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs. Nature 431:291Google Scholar
  7. Akunna JC, Bizeau C, Moletta R (1993) Nitrate and nitrite reductions with anaerobic sludge using various carbon sources: glucose, glycerol, acetic acid, lactic acid and methanol. Water Res 27:1303–1312Google Scholar
  8. Al-Bashir B, Cseh T, Leduc R, Samson R (1990) Effect of soil/contaminant interactions on the biodegradation of naphthalene in flooded soil under denitrifying conditions. Appl Microbiol Biotechnol 34:414–419Google Scholar
  9. Alejandro A-G, Ramon R-M, Silvia M (2013) Characterization of the anaerobic microbial community in oil-polluted subtidal sediments: aromatic biodegradation potential after the Prestige oil spill. Environ Microbiol 15:77–92Google Scholar
  10. Allamandola L, Tielens A, Barker J (1989) Interstellar polycyclic aromatic hydrocarbons - the infrared emission bands, the excitation/emission mechanism, and the astrophysical implications. Astrophys J Suppl Ser 71:733–775Google Scholar
  11. Ambrosoli R, Petruzzelli L, Minati JL, Marsan FA (2005) Anaerobic PAH degradation in soil by a mixed bacterial consortium under denitrifying conditions. Chemosphere 60:1231–1236Google Scholar
  12. Anderson RT, Lovley DR (1999) Naphthalene and benzene degradation under Fe(III)-reducing conditions in petroleum-contaminated aquifers. Biorem J 3:121–135Google Scholar
  13. Anderson RT, Lovley DR (2000) Anaerobic bioremediation of benzene under sulfate-reducing conditions in a petroleum-contaminated aquifer. Environ Sci Technol 34:2261–2266Google Scholar
  14. Andersson JT, Achten C (2015) Time to say goodbye to the 16 EPA PAHs? Toward an up-to-date use of PACs for environmental purposes. Polycyc Aromat Compd 35:330–354Google Scholar
  15. Annweiler E, Materna A, Safinowski M, Kappler A, Richnow HH, Michaelis W, Meckenstock RU (2000) Anaerobic degradation of 2-methylnaphthalene by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:5329–5333Google Scholar
  16. Annweiler E, Michaelis W, Meckenstock RU (2002) Identical ring cleavage products during anaerobic degradation of naphthalene, 2-methylnaphthalene, and tetralin indicate a new metabolic pathway. Appl Environ Microbiol 68:852–858Google Scholar
  17. Arthur EL, Rice PJ, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation – an overview. Crit Rev Plant Sci 24:109–122Google Scholar
  18. Azuma H, Toyota M, Asakawa Y, Kawano S (1996) Naphthalene – a constituent of Magnolia flowers. Phytochemistry 42:999–1004Google Scholar
  19. Bach Q-D, Kim S-J, Choi S-C, Oh Y-S (2005) Enhancing the intrinsic bioremediation of PAH-contaminated anoxic estuarine sediments with biostimulating agents. J Microbiol 43:319–324Google Scholar
  20. Bandowe BA, Meusel H (2017) Nitrated polycyclic aromatic hydrocarbons (nitro-PAHs) in the environment - a review. Sci Total Environ 581-582:237–257Google Scholar
  21. Barton LL, Fauque GD (2009) Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv Appl Microbiol 68:41–98Google Scholar
  22. Bauer JE, Capone DG (1985) Degradation and mineralization of the polycyclic aromatic hydrocarbons anthracene and naphthalene in intertidal marine sediments. Appl Environ Microbiol 50:81–90Google Scholar
  23. Bedessem ME, Swoboda-Colberg NG, Colberg PJ (1997) Naphthalene mineralization coupled to sulfate reduction in aquifer-derived enrichments. FEMS Microbiol Lett 152:213–218Google Scholar
  24. Beller HR, Spormann AM (1997) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J Bacteriol 179:670–676Google Scholar
  25. Berdugo-Clavijo C, Dong X, Soh J, Sensen CW, Gieg LM (2012) Methanogenic biodegradation of two-ringed polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol 81:124–133Google Scholar
  26. Bergmann F, Selesi D, Weinmaier T, Tischler P, Rattei T, Meckenstock RU (2011a) Genomic insights into the metabolic potential of the polycyclic aromatic hydrocarbon degrading sulfate-reducing Deltaproteobacterium N47. Environ Microbiol 13:1125–1137Google Scholar
  27. Bergmann FD, Selesi D, Meckenstock RU (2011b) Identification of new enzymes potentially involved in anaerobic naphthalene degradation by the sulfate-reducing enrichment culture N47. Arch Microbiol 193:241–250Google Scholar
  28. Biegert T, Fuchs G, Heider J (1996) Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur J Biochem 238:661–668Google Scholar
  29. Blumer M (1976) Polycyclic aromatic compounds in nature. Sci Am 234:34–45Google Scholar
  30. Blumer M, Youngblood WW (1975) Polycyclic aromatic hydrocarbons in soils and recent sediments. Science 188:53–55Google Scholar
  31. Boll M (2005) Dearomatizing benzene ring reductases. J Mol Microbiol Biotechnol 10:132–142Google Scholar
  32. Boll M, Fuchs G (1995) Benzoyl-coenzyme a reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism: ATP dependence of the reaction, purification and some properties of the enzyme from Thauera aromatica strain K172. Eur J Biochem 234:921–933Google Scholar
  33. Boll ES, Christensen JH, Holm PE (2008) Quantification and source identification of polycyclic aromatic hydrocarbons in sediment, soil, and water spinach from Hanoi, Vietnam. J Environ Monit 10:261–269Google Scholar
  34. Borneff J, Selenka F, Kunte H, Maximos A (1968) Experimental studies on the formation of polycyclic aromatic hydrocarbons in plants. Environ Res 2:22–29Google Scholar
  35. Breese K, Boll M, Alt-Morbe J, Schagger H, Fuchs G (1998) Genes coding for the benzoyl-CoA pathway of anaerobic aromatic metabolism in the bacterium Thauera aromatica. Eur J Biochem 256:148–154Google Scholar
  36. Brune A, Frenzel P, Cypionka H (2000) Life at the oxic–anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24:691–710Google Scholar
  37. Burdige DJ (2007) Preservation of organic matter in marine sediments: controls, mechanisms, and an imbalance in sediment organic carbon budgets? Chem Rev 107:467–485Google Scholar
  38. Burland SM, Edwards EA (1999) Anaerobic benzene biodegradation linked to nitrate reduction. Appl Environ Microbiol 65:529–533Google Scholar
  39. Cabrerizo A, Galbán-Malagón C, Del Vento S, Dachs J (2014) Sources and fate of polycyclic aromatic hydrocarbons in the Antarctic and Southern Ocean atmosphere. Glob Biogeochem Cycles 28:1424–1436Google Scholar
  40. Caldwell ME, Suflita JM (2000) Detection of phenol and benzoate as intermediates of anaerobic benzene biodegradation under different terminal electron-accepting conditions. Environ Sci Technol 34:1216–1220Google Scholar
  41. Callaghan AV (2013) Metabolomic investigations of anaerobic hydrocarbon-impacted environments. Curr Opin Biotechnol 24:506–515Google Scholar
  42. Canfield DE, Thamdrup B, Hansen JW (1993) The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim Cosmochim Acta 57:3867–3883Google Scholar
  43. Capone DG, Kiene RP (1988) Comparison of microbial dynamics in marine and freshwater sediments: contrasts in anaerobic carbon catabolism. Limnol Oceanogr 33:725–749Google Scholar
  44. Cappenberg TE (1974) Interrelations between sulfate-reducing and methane-producing bacteria in bottom deposits of a fresh-water lake. I. Field observations. Antonie Van Leeuwenhoek 40:285–295Google Scholar
  45. Cea-Barcia G, Carrère H, Steyer JP, Patureau D (2013) Evidence for PAH removal coupled to the first steps of anaerobic digestion in sewage sludge. Int J Chem Eng 2013:1–6.  https://doi.org/10.1155/2013/450542CrossRefGoogle Scholar
  46. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. In: Rosenberg E (ed) Microorganisms to combat pollution. Springer, Dordrecht, pp 227–244.  https://doi.org/10.1007/978-94-011-1672-5_16CrossRefGoogle Scholar
  47. Cerniglia C, Sutherland J (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2079–2110Google Scholar
  48. Cerniglia CE, Gibson DT, Van Baalen C (1979) Algal oxidation of aromatic hydrocarbons: formation of 1-naphthol from naphthalene by Agmenellum quadruplicatum, strain PR-6. Biochem Biophys Res Commun 88:50–58Google Scholar
  49. Cerniglia CE, Van Baalen C, Gibson DT (1980) Metabolism of naphthalene by the cyanobacterium Oscillatoria sp., strain JCM. Microbiology 116:485–494Google Scholar
  50. Chang W, Jones TN, Holoman TRP (2001) Anaerobic polycyclic aromatic hydrocarbon(PAH)-degrading enrichment cultures under methanogenic conditions. In: Sixth international in situ and on site bioremediation symposium, pp 205–209Google Scholar
  51. Chang B, Shiung L, Yuan S (2002) Anaerobic biodegradation of polycyclic aromatic hydrocarbon in soil. Chemosphere 48:717–724Google Scholar
  52. Chang B, Chang S, Yuan S (2003) Anaerobic degradation of polycyclic aromatic hydrocarbons in sludge. Adv Environ Res 7:623–628Google Scholar
  53. Chang W, Um Y, Hoffman B, Holoman TRP (2005) Molecular characterization of polycyclic aromatic hydrocarbon (PAH)-degrading methanogenic communities. Biotechnol Prog 21:682–688Google Scholar
  54. Chang W, Um Y, Holoman TRP (2006) Polycyclic aromatic hydrocarbon (PAH) degradation coupled to methanogenesis. Biotechnol Lett 28:425–430Google Scholar
  55. Chang B-V, Chang IT, Yuan SY (2008) Anaerobic degradation of phenanthrene and pyrene in mangrove sediment. Bull Environ Contam Toxicol 80:145–149Google Scholar
  56. Christensen N, Batstone DJ, He Z, Angelidaki I, Schmidt J (2004) Removal of polycyclic aromatic hydrocarbons (PAHs) from sewage sludge by anaerobic degradation. Water Sci Technol 50:237–244Google Scholar
  57. Coates JD, Anderson RT, Lovley DR (1996) Oxidation of polycyclic aromatic hydrocarbons under sulfate-reducing conditions. Appl Environ Microbiol 62:1099–1101Google Scholar
  58. Coates JD, Woodward J, Allen J, Philp P, Lovley DR (1997) Anaerobic degradation of polycyclic aromatic hydrocarbons and alkanes in petroleum-contaminated marine harbor sediments. Appl Environ Microbiol 63:3589–3593Google Scholar
  59. Coates JD, Chakraborty R, Lack JG, O’connor SM, Cole KA, Bender KS, Achenbach LA (2001) Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411:1039Google Scholar
  60. Coates JD, Chakraborty R, McInerney MJ (2002) Anaerobic benzene biodegradation – a new era. Res Microbiol 153:621–628Google Scholar
  61. Cohen M, Barlow MJ (2005) Polycyclic aromatic hydrocarbon emission bands in selected planetary nebulae: a study of the behaviour with gas phase C/O ratio. Mon Not R Astron Soc 362:1199–1207Google Scholar
  62. Cunningham JA, Rahme H, Hopkins GD, Lebron C, Reinhard M (2001) Enhanced in situ bioremediation of BTEX-contaminated groundwater by combined injection of nitrate and sulfate. Environ Sci Technol 35:1663–1670Google Scholar
  63. Daisy BH, Strobel GA, Castillo U, Ezra D, Sears J, Weaver DK, Runyon JB (2002) Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148:3737–3741Google Scholar
  64. Davidova IA, Gieg LM, Duncan KE, Suflita JM (2007) Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. ISME J 1:436–442Google Scholar
  65. Deziel E, Paquette G, Villemur R, Lepine F, Bisaillon J (1996) Biosurfactant production by a soil Pseudomonas strain growing on polycyclic aromatic hydrocarbons. Appl Environ Microbiol 62:1908–1912Google Scholar
  66. Didonato RJ Jr et al (2010) Genome sequence of the deltaproteobacterial strain Naphs2 and analysis of differential gene expression during anaerobic growth on naphthalene. PLoS One 5(11):e14072Google Scholar
  67. Dolfing J, Xu A, Gray ND, Larter SR, Head IM (2009) The thermodynamic landscape of methanogenic PAH degradation. Microb Biotechnol 2:566–574Google Scholar
  68. Dou J, Liu X, Ding A (2009) Anaerobic degradation of naphthalene by the mixed bacteria under nitrate reducing conditions. J Hazard Mater 165:325–331Google Scholar
  69. Drew MC (1990) Sensing soil oxygen. Plant Cell Environ 13:681–693Google Scholar
  70. Duran R, Cravo-Laureau C (2016) Role of environmental factors and microorganisms in determining the fate of polycyclic aromatic hydrocarbons in the marine environment. FEMS Microbiol Rev 40:814–830Google Scholar
  71. Eberlein C, Estelmann S, Seifert J, Von Bergen M, Müller M, Meckenstock RU, Boll M (2013a) Identification and characterization of 2-naphthoyl-coenzyme A reductase, the prototype of a novel class of dearomatizing reductases. Mol Microbiol 88:1032–1039Google Scholar
  72. Eberlein C, Johannes J, Mouttaki H, Sadeghi M, Golding BT, Boll M, Meckenstock RU (2013b) ATP-dependent/−independent enzymatic ring reductions involved in the anaerobic catabolism of naphthalene. Environ Microbiol 15:1832–1841Google Scholar
  73. Edwards E, Wills L, Reinhard M, Grbić-Galić D (1992) Anaerobic degradation of toluene and xylene by aquifer microorganisms under sulfate-reducing conditions. Appl Environ Microbiol 58:794–800Google Scholar
  74. Egland PG, Pelletier DA, Dispensa M, Gibson J, Harwood CS (1997) A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc Natl Acad Sci U S A 94:6484–6489Google Scholar
  75. Eriksson M, Sodersten E, Yu Z, Dalhammar G, Mohn WW (2003) Degradation of polycyclic aromatic hydrocarbons at low temperature under aerobic and nitrate-reducing conditions in enrichment cultures from northern soils. Appl Environ Microbiol 69:275–284Google Scholar
  76. Estelmann S, Blank I, Feldmann A, Boll M (2015) Two distinct old yellow enzymes are involved in naphthyl ring reduction during anaerobic naphthalene degradation. Mol Microbiol 95:162–172Google Scholar
  77. Ezra D, Hess WM, Strobel GA (2004) New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiology 150:4023–4031Google Scholar
  78. Fernández P, Grimalt JO (2003) On the global distribution of persistent organic pollutants. Chimia 57:514–521Google Scholar
  79. Ferrarese E, Andreottola G, Oprea IA (2008) Remediation of PAH-contaminated sediments by chemical oxidation. J Hazard Mater 152:128–139Google Scholar
  80. Foght J (2008) Anaerobic biodegradation of aromatic hydrocarbons: pathways and prospects. J Mol Microbiol Biotechnol 15:93–120Google Scholar
  81. Folwell BD, McGenity TJ, Price A, Johnson RJ, Whitby C (2016) Exploring the capacity for anaerobic biodegradation of polycyclic aromatic hydrocarbons and naphthenic acids by microbes from oil-sands-process-affected waters. Int Biodeterior Biodegrad 108:214–221Google Scholar
  82. Frey PA, Reed GH (2012) The ubiquity of iron. ACS Chem Biol 7:1477–1481Google Scholar
  83. Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds - from one strategy to four. Nat Rev Microbiol 9:803–816Google Scholar
  84. Galushko A, Minz D, Schink B, Widdel F (1999) Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environ Microbiol 1:415–420Google Scholar
  85. Gieg LM, Toth CR (2017) Signature metabolite analysis to determine in situ anaerobic hydrocarbon biodegradation. In: Boll M (ed) Anaerobic utilization of hydrocarbons, oils, and lipids, Handbook of hydrocarbon and lipid microbiology. Springer, Cham, pp 1–30Google Scholar
  86. Gieg LM, Duncan KE, Suflita JM (2008) Bioenergy production via microbial conversion of residual oil to natural gas. Appl Environ Microbiol 74:3022–3029Google Scholar
  87. Griebler C, Safinowski M, Vieth A, Richnow HH, Meckenstock RU (2004) Combined application of stable carbon isotope analysis and specific metabolites determination for assessing in situ degradation of aromatic hydrocarbons in a tar oil-contaminated aquifer. Environ Sci Technol 38:617–631Google Scholar
  88. Grimmer G, Jacob J, Naujack K-W (1983) Profile of the polycyclic aromatic compounds from crude oils. Fresenius Z Anal Chem 314:29–36Google Scholar
  89. Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243Google Scholar
  90. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15Google Scholar
  91. Harwood CS, Burchhardt G, Herrmann H, Fuchs G (1998) Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol Rev 22:439–458Google Scholar
  92. Hayakawa K (2018) Oil spills and polycyclic aromatic hydrocarbons. In: Hayakawa K (ed) Polycyclic aromatic hydrocarbons: environmental behavior and toxicity in East Asia. Springer, Singapore, pp 213–223.  https://doi.org/10.1007/978-981-10-6775-4_16CrossRefGoogle Scholar
  93. Hayes LA, Nevin KP, Lovley DR (1999) Role of prior exposure on anaerobic degradation of naphthalene and phenanthrene in marine harbor sediments. Org Geochem 30:937–945Google Scholar
  94. Haynes WM (2014) CRC handbook of chemistry and physics. CRC Press, Boca RatonGoogle Scholar
  95. Hazen TC (2010) Cometabolic bioremediation. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2505–2514.  https://doi.org/10.1007/978-3-540-77587-4_185CrossRefGoogle Scholar
  96. Himmelberg AM, Brüls T, Farmani Z, Weyrauch P, Barthel G, Schrader W, Meckenstock RU (2018) Anaerobic degradation of phenanthrene by a sulfate-reducing enrichment culture. Environ Microbiol 20:3589–3600Google Scholar
  97. Hong Y-W, Yuan D-X, Lin Q-M, Yang T-L (2008) Accumulation and biodegradation of phenanthrene and fluoranthene by the algae enriched from a mangrove aquatic ecosystem. Mar Pollut Bull 56:1400–1405Google Scholar
  98. IARC (2010) Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr Eval Carcinog Risks Hum 92:1Google Scholar
  99. Jahn MK, Haderlein SB, Meckenstock RU (2005) Anaerobic degradation of benzene, toluene, ethylbenzene, and o-xylene in sediment-free iron-reducing enrichment cultures. Appl Environ Microbiol 71:3355–3358Google Scholar
  100. Joback KG, Reid RC (1987) Estimation of pure-component properties from group-contributions. Chem Eng Commun 57:233–243Google Scholar
  101. Jobelius C, Ruth B, Griebler C, Meckenstock RU, Hollender J, Reineke A, Frimmel FH, Zwiener C (2010) Metabolites indicate hot spots of biodegradation and biogeochemical gradients in a high-resolution monitoring well. Environ Sci Technol 45:474–481Google Scholar
  102. Johann H, Georg F (1997) Anaerobic metabolism of aromatic compounds. Eur J Biochem 243:577–596Google Scholar
  103. Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84Google Scholar
  104. Johnson K, Ghosh S (1998) Feasibility of anaerobic biodegradation of PAHs in dredged river sediments. Water Sci Technol 38:41–48Google Scholar
  105. Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:57–88Google Scholar
  106. Kaiho K (1994) Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen levels in the modern ocean. Geology 22:719–722Google Scholar
  107. Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067Google Scholar
  108. Karavalakis G, Deves G, Fontaras G, Stournas S, Samaras Z, Bakeas E (2010) The impact of soy-based biodiesel on PAH, nitro-PAH and oxy-PAH emissions from a passenger car operated over regulated and nonregulated driving cycles. Fuel 89:3876–3883Google Scholar
  109. Karickhoff SW, Brown DS, Scott TA (1979) Sorption of hydrophobic pollutants on natural sediments. Water Res 13:241–248Google Scholar
  110. Kim K-H, Jahan SA, Kabir E, Brown RJ (2013) A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environ Int 60:71–80Google Scholar
  111. Kirso U, Irha N (1998) Role of algae in fate of carcinogenic polycyclic aromatic hydrocarbons in the aquatic environment. Ecotoxicol Environ Saf 41:83–89Google Scholar
  112. Kleemann R, Meckenstock RU (2011) Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria. FEMS Microbiol Ecol 78:488–496Google Scholar
  113. Kobayashi H, Rittmann BE (1982) Microbial removal of hazardous organic compounds. Environ Sci Technol 16:170A–183AGoogle Scholar
  114. Kraft B, Tegetmeyer H, Sharma R, Klotz M, Ferdelman T, Hettich R, Geelhoed J, Strous M (2014) The environmental controls that govern the end product of bacterial nitrate respiration. Science 345:676–679Google Scholar
  115. Kukučka P, Lammel G, Dvorská A, Klánová J, Möller A, Fries E (2010) Contamination of Antarctic snow by polycyclic aromatic hydrocarbons dominated by combustion sources in the polar region. Environ Chem 7:504–513Google Scholar
  116. Kummel S et al (2015) Anaerobic naphthalene degradation by sulfate-reducing Desulfobacteraceae from various anoxic aquifers. FEMS Microbiol Ecol 91(3):fiv006Google Scholar
  117. Kung JW et al (2009) Identification and characterization of the tungsten-containing class of benzoyl-coenzyme A reductases. Proc Natl Acad Sci U S A 106:17687–17692Google Scholar
  118. Kuppusamy S, Thavamani P, Venkateswarlu K, Lee YB, Naidu R, Megharaj M (2017) Remediation approaches for polycyclic aromatic hydrocarbons (PAHs) contaminated soils: technological constraints, emerging trends and future directions. Chemosphere 168:944–968Google Scholar
  119. Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263Google Scholar
  120. Laflamme RE, Hites RA (1978) The global distribution of polycyclic aromatic hydrocarbons in recent sediments. Geochim Cosmochim Acta 42:289–303Google Scholar
  121. Landrum P, Giesy J, Oris J, Allred P (1986) Photoinduced toxicity of polycyclic aromatic hydrocarbons to aquatic organisms. In: Vandermuelen J, Hrudey S (eds) Oil in freshwater: chemistry, biology, countermeasure technology. Pergamon Press, Elmsford, pp 304–318Google Scholar
  122. Langenhoff AAM, Zehnder AJB, Schraa G (1996) Behaviour of toluene, benzene and naphthalene under anaerobic conditions in sediment columns. Biodegradation 7:267–274Google Scholar
  123. Latimer J, Zheng J (2003) The sources, transport and fate of PAHs in the marine environment. In: Douben P (ed) PAHs: an ecotoxicological perspective. Wiley, West Sussex, pp 7–53Google Scholar
  124. Leduc R, Samson R, Al-Bashir B, Al-Hawari J, Cseh T (1992) Biotic and abiotic disappearance of four pah compounds from flooded soil under various redox conditions. Water Sci Technol 26:51–60Google Scholar
  125. Lei A, Wong Y, Tam N (2002) Removal of pyrene by different microalgal species. Water Sci Technol 46:195–201Google Scholar
  126. Li C-H, Zhou H-W, Wong Y-S, Tam NF-Y (2009) Vertical distribution and anaerobic biodegradation of polycyclic aromatic hydrocarbons in mangrove sediments in Hong Kong, South China. Sci Total Environ 407:5772–5779Google Scholar
  127. Li CH, Ye C, Wong YS, Tam NF (2011) Effect of Mn(IV) on the biodegradation of polycyclic aromatic hydrocarbons under low-oxygen condition in mangrove sediment slurry. J Hazard Mater 190:786–793Google Scholar
  128. Li C, Wong Y, Wang H, Tam N (2015) Anaerobic biodegradation of PAHs in mangrove sediment with amendment of NaHCO3. J Environ Sci 30:148–156Google Scholar
  129. Liang L, Song X, Kong J, Shen C, Huang T, Hu Z (2014) Anaerobic biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by a facultative anaerobe Pseudomonas sp. JP1. Biodegradation 25:825–833Google Scholar
  130. Lima ALC, Farrington JW, Reddy CM (2005) Combustion-derived polycyclic aromatic hydrocarbons in the environment – a review. Environ Forensic 6:109–131Google Scholar
  131. Lovley DR (2001) Anaerobes to the rescue. Science 293:1444–1446Google Scholar
  132. Lovley DR, Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol, and p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl Environ Microbiol 56:1858–1864Google Scholar
  133. Lovley DR, Woodward JC, Chapelle FH (1994) Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe (III) ligands. Nature 370:128Google Scholar
  134. Lovley DR, Coates JD, Woodward JC, Phillips E (1995) Benzene oxidation coupled to sulfate reduction. Appl Environ Microbiol 61:953–958Google Scholar
  135. Lu X, Zhang T, Fang HH-P, Leung KM, Zhang G (2011) Biodegradation of naphthalene by enriched marine denitrifying bacteria. Int Biodeterior Biodegrad 65:204–211Google Scholar
  136. Lu X-Y, Li B, Zhang T, Fang HH (2012) Enhanced anoxic bioremediation of PAHs-contaminated sediment. Bioresour Technol 104:51–58Google Scholar
  137. Lundstedt S et al (2007) Sources, fate, and toxic hazards of oxygenated polycyclic aromatic hydrocarbons (PAHs) at PAH-contaminated sites. Ambio 36:475–485Google Scholar
  138. Luo L, Wang P, Lin L, Luan T, Ke L, Tam NFY (2014) Removal and transformation of high molecular weight polycyclic aromatic hydrocarbons in water by live and dead microalgae. Process Biochem 49:1723–1732Google Scholar
  139. Luo L, Lai X, Chen B, Lin L, Fang L, Tam NF, Luan T (2015) Chlorophyll catalyse the photo-transformation of carcinogenic benzo[a]pyrene in water. Sci Rep 5:12776Google Scholar
  140. Ma B, He Y, Chen H-H, Xu J-M, Rengel Z (2010) Dissipation of polycyclic aromatic hydrocarbons (PAHs) in the rhizosphere: synthesis through meta-analysis. Environ Pollut 158:855–861Google Scholar
  141. Ma C, Wang Y, Zhuang L, Huang D, Zhou S, Li F (2011) Anaerobic degradation of phenanthrene by a newly isolated humus-reducing bacterium, Pseudomonas aeruginosa strain PAH-1. J Soils Sed 11:923–929Google Scholar
  142. MacRae JD, Hall KJ (1998) Biodegradation of polycyclic aromatic hydrocarbons (PAH) in marine sediment under denitrifying conditions. Water Sci Technol 38:177–185Google Scholar
  143. Majora DW, Mayfielda CI, Barkerb JF (1988) Biotransformation of benzene by denitrification in aquifer sand. Groundwater 26:8–14Google Scholar
  144. Maliszewska-Kordybach B (1999) Sources, concentrations, fate and effects of polycyclic aromatic hydrocarbons (PAHs) in the environment. Part A: PAHs in air. Pol J Environ Stud 8:131–136Google Scholar
  145. Margulis L, Sagan D (1997) Microcosmos: four billion years of microbial evolution. University of California Press, New YorkGoogle Scholar
  146. Marozava S, Mouttaki H, Muller H, Abu Laban N, Probst AJ, Meckenstock RU (2018) Anaerobic degradation of 1-methylnaphthalene by a member of the Thermoanaerobacteraceae contained in an iron-reducing enrichment culture. Biodegradation 29:23–39Google Scholar
  147. Martens CS, Val Klump J (1984) Biogeochemical cycling in an organic-rich coastal marine basin 4. An organic carbon budget for sediments dominated by sulfate reduction and methanogenesis. Geochim Cosmochim Acta 48:1987–2004Google Scholar
  148. Martirani-Von Abercron S-M, Pacheco D, Benito-Santano P, Marín P, Marqués S (2016) Polycyclic aromatic hydrocarbon-induced changes in bacterial community structure under anoxic nitrate reducing conditions. Front Microbiol 7:1775Google Scholar
  149. McInerney MJ, Sieber JR, Gunsalus RP (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20:623–632Google Scholar
  150. McNally DL, Mihelcic JR, Lueking DR (1998) Biodegradation of three-and four-ring polycyclic aromatic hydrocarbons under aerobic and denitrifying conditions. Environ Sci Technol 32:2633–2639Google Scholar
  151. McNeely RN, Neimanis VP, Dwyer L (1979) Water quality sourcebook: a guide to water quality parameters. Waters Directorate, Water Quality Branch, OttawaGoogle Scholar
  152. Means JC, Wood SG, Hassett JJ, Banwart WL (1980) Sorption of polynuclear aromatic hydrocarbons by sediments and soils. Environ Sci Technol 14:1524–1528Google Scholar
  153. Meckenstock RU, Mouttaki H (2011) Anaerobic degradation of non-substituted aromatic hydrocarbons. Curr Opin Biotechnol 22:406–414Google Scholar
  154. Meckenstock RU, Annweiler E, Michaelis W, Richnow HH, Schink B (2000) Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:2743–2747Google Scholar
  155. Meckenstock RU, Safinowski M, Griebler C (2004) Anaerobic degradation of polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol 49:27–36Google Scholar
  156. Meckenstock RU et al (2016) Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons. J Mol Microbiol Biotechnol 26:92–118Google Scholar
  157. Menzie CA, Potocki BB, Santodonato J (1992) Exposure to carcinogenic PAHs in the environment. Environ Sci Technol 26:1278–1284Google Scholar
  158. Mihelcic JR, Luthy RG (1988a) Degradation of polycyclic aromatic hydrocarbon compounds under various redox conditions in soil-water systems. Appl Environ Microbiol 54:1182–1187Google Scholar
  159. Mihelcic JR, Luthy RG (1988b) Microbial degradation of acenaphthene and naphthalene under denitrification conditions in soil-water systems. Appl Environ Microbiol 54:1188–1198Google Scholar
  160. Miki S, Uno S, Ito K, Koyama J, Tanaka H (2014) Distributions of polycyclic aromatic hydrocarbons and alkylated polycyclic aromatic hydrocarbons in Osaka Bay, Japan. Mar Pollut Bull 85:558–565Google Scholar
  161. Miller JS, Olejnik D (2001) Photolysis of polycyclic aromatic hydrocarbons in water. Water Res 35:233–243Google Scholar
  162. Miller MM, Wasik SP, Huang GL, Shiu WY, Mackay D (1985) Relationships between octanol-water partition coefficient and aqueous solubility. Environ Sci Technol 19:522–529Google Scholar
  163. Morgan P, Watkinson RJ (1992) Factors limiting the supply and efficiency of nutrient and oxygen supplements for the in situ biotreatment of contaminated soil and groundwater. Water Res 26:73–78Google Scholar
  164. Mouttaki H, Johannes J, Meckenstock RU (2012) Identification of naphthalene carboxylase as a prototype for the anaerobic activation of non-substituted aromatic hydrocarbons. Environ Microbiol 14:2770–2774Google Scholar
  165. Mulas G, Malloci G, Joblin C, Toublanc D (2006) Estimated IR and phosphorescence emission fluxes for specific polycyclic aromatic hydrocarbons in the red rectangle. A&A 446:537–549Google Scholar
  166. Müller JA, Schink B (2000) Initial steps in the fermentation of 3-hydroxybenzoate by Sporotomaculum hydroxybenzoicum. Arch Microbiol 173:288–295Google Scholar
  167. Mulligan CN (2005) Environmental applications for biosurfactants. Environ Pollut 133:183–198Google Scholar
  168. Murphy T, Moller A, Brouwer H (1995) In situ treatment of Hamilton Harbour sediment. Aquat Ecosyst Health Manag 4:195–203Google Scholar
  169. Musat F et al (2009) Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environ Microbiol 11:209–219Google Scholar
  170. Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441Google Scholar
  171. Nales M, Butler BJ, Edwards EA (1998) Anaerobic benzene biodegradation: a microcosm survey. Biorem J 2:125–144Google Scholar
  172. Neilson AN (2013) PAHs and related compounds: chemistry, vol 3. Springer, BerlinGoogle Scholar
  173. Neilson A, Allard A, Remberger M (1998) The handbook of environmental chemistry. Part J. PAHs and related compounds. Springer, BerlinGoogle Scholar
  174. Nestler FHM (1974) Characterization of wood-preserving coal-tar creosote by gas-liquid chromatography. Anal Chem 46:46–53Google Scholar
  175. Nielsen T, Ramdahl T, Bjørseth A (1983) The fate of airborne polycyclic organic matter. Environ Health Perspect 47:103Google Scholar
  176. Nisbet EG, Sleep NH (2001) The habitat and nature of early life. Nature 409:1083Google Scholar
  177. Northrop D, Simpson O, Mott N (1956) Electronic properties of aromatic hydrocarbons I. Electrical conductivity. Proc R Soc Lond A 234:124–135Google Scholar
  178. O’Neil MJ (2013) The Merck index: an encyclopedia of chemicals, drugs, and biologicals. RSC Publishing, LondonGoogle Scholar
  179. Ohlenbusch G, Zwiener C, Meckenstock RU, Frimmel FH (2002) Identification and quantification of polar naphthalene derivatives in contaminated groundwater of a former gas plant site by liquid chromatography–electrospray ionization tandem mass spectrometry. J Chromatogr 967:201–207Google Scholar
  180. Ohura T (2007) Environmental behavior, sources, and effects of chlorinated polycyclic aromatic hydrocarbons. Sci World J 7:372–380Google Scholar
  181. Oka AR, Phelps CD, Zhu X, Saber DL, Young L (2011) Dual biomarkers of anaerobic hydrocarbon degradation in historically contaminated groundwater. Environ Sci Technol 45:3407–3414Google Scholar
  182. Okere U, Semple K (2012) Biodegradation of PAHs in ‘pristine’soils from different climatic regions. J Bioremed Biodegr S1:006Google Scholar
  183. Oko BJ, Tao Y, Stuckey DC (2017) Dynamics of two methanogenic microbiomes incubated in polycyclic aromatic hydrocarbons, naphthenic acids, and oil field produced water. Biotechnol Biofuels 10:1–13Google Scholar
  184. Ou S, Zheng J, Zheng J, Richardson BJ, Lam PK (2004) Petroleum hydrocarbons and polycyclic aromatic hydrocarbons in the surficial sediments of Xiamen Harbour and Yuan Dan Lake, China. Chemosphere 56:107–112Google Scholar
  185. Page DS, Brown JS, Boehm PD, Bence AE, Neff JM (2006) A hierarchical approach measures the aerial extent and concentration levels of PAH-contaminated shoreline sediments at historic industrial sites in Prince William Sound, Alaska. Mar Pollut Bull 52:367–379Google Scholar
  186. Parisi VA, Brubaker GR, Zenker MJ, Prince RC, Gieg LM, Da Silva MLB, Alvarez PJJ, Suflita JM (2009) Field metabolomics and laboratory assessments of anaerobic intrinsic bioremediation of hydrocarbons at a petroleum-contaminated site. Microb Biotechnol 2:202–212Google Scholar
  187. Peeters E (2011) The PAH hypothesis after 25 years. Proc Int Astron Union 7:149–161Google Scholar
  188. Peng R-H et al (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955Google Scholar
  189. Perelo LW (2010) In situ and bioremediation of organic pollutants in aquatic sediments. J Hazard Mater 177:81–89Google Scholar
  190. Phelps CD, Battistelli J, Young L (2002) Metabolic biomarkers for monitoring anaerobic naphthalene biodegradation in situ. Environ Microbiol 4:532–537Google Scholar
  191. Phelps CD, Kazumi J, Young LY (1996) Anaerobic degradation of benzene in BTX mixtures dependent on sulfate reduction. FEMS Microbiol Lett 145:433–437Google Scholar
  192. Planavsky NJ et al (2014) Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat Geosci 7:283Google Scholar
  193. Qin W, Zhu Y, Fan F, Wang Y, Liu X, Ding A, Dou J (2017) Biodegradation of benzo(a)pyrene by Microbacterium sp. strain under denitrification: degradation pathway and effects of limiting electron acceptors or carbon source. Biochem Eng J 121:131–138Google Scholar
  194. Qin W, Fan F, Zhu Y, Huang X, Ding A, Liu X, Dou J (2018) Anaerobic biodegradation of benzo(a)pyrene by a novel Cellulosimicrobium cellulans CWS2 isolated from polycyclic aromatic hydrocarbon-contaminated soil. Braz J Microbiol 49:258–268Google Scholar
  195. Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F, Reinhardt R (2005) The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183:27–36Google Scholar
  196. Rafin C, Potin O, Veignie E, Sahraoui L-HA, Sancholle M (2000) Degradation of Benzo[a]Pyrene as sole carbon source by a non white rot fungus, Fusarium solani. Polycyc Aromat Compd 21:311–329Google Scholar
  197. Ribeiro H et al (2018) Potential of dissimilatory nitrate reduction pathways in polycyclic aromatic hydrocarbon degradation. Chemosphere 199:54–67Google Scholar
  198. Rochman CM, Manzano C, Hentschel BT, Simonich SLM, Hoh E (2013) Polystyrene plastic: a source and sink for polycyclic aromatic hydrocarbons in the marine environment. Environ Sci Technol 47:13976–13984Google Scholar
  199. Rockne KJ, Strand SE (1998) Biodegradation of bicyclic and polycyclic aromatic hydrocarbons in anaerobic enrichments. Environ Sci Technol 32:3962–3967Google Scholar
  200. Rockne KJ, Strand SE (2001) Anaerobic biodegradation of naphthalene, phenanthrene, and biphenyl by a denitrifying enrichment culture. Water Res 35:291–299Google Scholar
  201. Rockne KJ, Chee-Sanford JC, Sanford RA, Hedlund BP, Staley JT, Strand SE (2000) Anaerobic naphthalene degradation by microbial pure cultures under nitrate-reducing conditions. Appl Environ Microbiol 66:1595–1601Google Scholar
  202. Ron EZ, Rosenberg E (2002) Biosurfactants and oil bioremediation. Curr Opin Biotechnol 13:249–252Google Scholar
  203. Ross AB et al (2002) Measurement and prediction of the emission of pollutants from the combustion of coal and biomass in a fixed bed furnace. Fuel 81:571–582Google Scholar
  204. Rothermich MM, Hayes LA, Lovley DR (2002) Anaerobic, sulfate-dependent degradation of polycyclic aromatic hydrocarbons in petroleum-contaminated harbor sediment. Environ Sci Technol 36:4811–4817Google Scholar
  205. Safinowski M, Meckenstock RU (2004) Enzymatic reactions in anaerobic 2-methylnaphthalene degradation by the sulphate-reducing enrichment culture N47. FEMS Microbiol Lett 240:99–104Google Scholar
  206. Safinowski M, Meckenstock RU (2006) Methylation is the initial reaction in anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Environ Microbiol 8:347–352Google Scholar
  207. Safinowski M, Griebler C, Meckenstock RU (2006) Anaerobic cometabolic transformation of polycyclic and heterocyclic aromatic hydrocarbons: evidence from laboratory and field studies. Environ Sci Technol 40:4165–4173Google Scholar
  208. Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243–248Google Scholar
  209. Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280Google Scholar
  210. Schöcke L, Schink B (1999) Energetics and biochemistry of fermentative benzoate degradation by Syntrophus gentianae. Arch Microbiol 171:331–337Google Scholar
  211. Schoeny R, Cody T, Warshawsky D, Radike M (1988) Metabolism of mutagenic polycyclic aromatic hydrocarbons by photosynthetic algal species. Mutat Res 197:289–302Google Scholar
  212. Schühle K, Gescher J, Feil U, Paul M, Jahn M, Schägger H, Fuchs G (2003) Benzoate-coenzyme A ligase from Thauera aromatica: an enzyme acting in anaerobic and aerobic pathways. J Bacteriol 185:4920–4929Google Scholar
  213. Selesi D et al (2010) Combined genomic and proteomic approaches identify gene clusters involved in anaerobic 2-methylnaphthalene degradation in the sulfate-reducing enrichment culture N47. J Bacteriol 192:295–306Google Scholar
  214. Sharak Genthner BR, Townsend GT, Lantz SE, Mueller JG (1997) Persistence of polycyclic aromatic hydrocarbon components of creosote under anaerobic enrichment conditions. Arch Environ Contam Toxicol 32:99–105Google Scholar
  215. Shen G, Tao S, Wei S, Zhang Y, Wang R, Wang B, Li W, Shen H, Huang Y, Chen Y, Chen H, Yang Y, Wang W, Wang X, Liu W, Simonich SLM (2012) Emissions of parent, nitro, and oxygenated polycyclic aromatic hydrocarbons from residential wood combustion in rural China. Environ Sci Technol 46:8123–8130Google Scholar
  216. Sims RC, Overcash MR (1983) Fate of polynuclear aromatic compounds (PNAs) in soil-plant systems. Residue Rev 88:1–68Google Scholar
  217. Sivaram AK, Logeshwaran P, Subashchandrabose SR, Lockington R, Naidu R, Megharaj M (2018) Comparison of plants with C3 and C4 carbon fixation pathways for remediation of polycyclic aromatic hydrocarbon contaminated soils. Sci Rep 8:2100Google Scholar
  218. Skupinska K, Misiewicz I, Kasprzycka-Guttman T (2004) Polycyclic aromatic hydrocarbons: physicochemical properties, environmental appearance and impact on living organisms. Acta Pol Pharm 61:233–240Google Scholar
  219. Smith MB, March J (2007) March’s advanced organic chemistry: reactions, mechanisms, and structure. Wiley, HobokenGoogle Scholar
  220. Sporstol S, Gjos N, Lichtenthaler RG, Gustavsen KO, Urdal K, Oreld F, Skei J (1983) Source identification of aromatic hydrocarbons in sediments using GC/MS. Environ Sci Technol 17:282–286Google Scholar
  221. Stein SE, Fahr A (1985) High-temperature stabilities of hydrocarbons. J Phys Chem 89:3714–3725Google Scholar
  222. Stogiannidis E, Laane R (2015) Source characterization of polycyclic aromatic hydrocarbons by using their molecular indices: an overview of possibilities. Rev Environ Contam Toxicol 234:49–133Google Scholar
  223. Subashchandrabose SR, Krishnan K, Gratton E, Megharaj M, Naidu R (2014) Potential of fluorescence imaging techniques to monitor mutagenic PAH uptake by microalga. Environ Sci Technol 48:9152–9160Google Scholar
  224. Subashchandrabose SR, Logeshwaran P, Venkateswarlu K, Naidu R, Megharaj M (2017) Pyrene degradation by Chlorella sp. MM3 in liquid medium and soil slurry: possible role of dihydrolipoamide acetyltransferase in pyrene biodegradation. Algal Res 23:223–232Google Scholar
  225. Sullivan ER, Zhang X, Phelps C, Young L (2001) Anaerobic mineralization of stable-isotope-labeled 2-methylnaphthalene. Appl Environ Microbiol 67:4353–4357Google Scholar
  226. Sutherland JB, Freeman JP, Selby AL, Fu PP, Miller DW, Cerniglia CE (1990) Stereoselective formation of a K-region dihydrodiol from phenanthrene by Streptomyces flavovirens. Arch Microbiol 154:260–266Google Scholar
  227. Sutton MA, Oenema O, Erisman JW, Leip A, van Grinsven H, Winiwarter W (2011) Too much of a good thing. Nature 472:159Google Scholar
  228. Tang YJ, Carpenter S, Deming J, Krieger-Brockett B (2005) Controlled release of nitrate and sulfate to enhance anaerobic bioremediation of phenanthrene in marine sediments. Environ Sci Technol 39:3368–3373Google Scholar
  229. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180Google Scholar
  230. Thomas J, Ward C (1989) In situ biorestoration of organic contaminants in the subsurface. Environ Sci Technol 23:760–766Google Scholar
  231. Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1983) Denitrification: ecological niches, competition and survival. Antonie Van Leeuwenhoek 48:569–583Google Scholar
  232. Tielens AG (2005) The physics and chemistry of the interstellar medium. Cambridge University Press, Cambridge.  https://doi.org/10.1017/CBO9780511819056CrossRefGoogle Scholar
  233. Tongpim S, Pickard MA (1999) Cometabolic oxidation of phenanthrene to phenanthrene trans-9, 10-dihydrodiol by Mycobacterium strain S1 growing on anthracene in the presence of phenanthrene. Can J Microbiol 45:369–376Google Scholar
  234. Toth CRA, Berdugo-Clavijo C, O’Farrell CM, Jones GM, Sheremet A, Dunfield PF, Gieg LM (2018) Stable isotope and metagenomic profiling of a methanogenic naphthalene-degrading enrichment culture. Microorganisms 6(3):E65Google Scholar
  235. Townsend GT, Prince RC, Suflita JM (2003) Anaerobic oxidation of crude oil hydrocarbons by the resident microorganisms of a contaminated anoxic aquifer. Environ Sci Technol 37:5213–5218Google Scholar
  236. Trably E, Patureau D, Delgenes J (2003) Enhancement of polycyclic aromatic hydrocarbons removal during anaerobic treatment of urban sludge. Water Sci Technol 48:53–60Google Scholar
  237. Tsai J-C, Kumar M, Lin J-G (2009) Anaerobic biotransformation of fluorene and phenanthrene by sulfate-reducing bacteria and identification of biotransformation pathway. J Hazard Mater 164:847–855Google Scholar
  238. Tsibart A, Gennadiev A, Koshovskii T, Watts A (2014) Polycyclic aromatic hydrocarbons in post-fire soils of drained peatlands in western Meshchera (Moscow region, Russia). Solid Earth 5:1305–1317Google Scholar
  239. Tu Q et al (2014) GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis. Mol Ecol Resour 14:914–928Google Scholar
  240. Tuyen LH, Tue NM, Takahashi S, Suzuki G, Viet PH, Subramanian A, Bulbule KA, Parthasarathy P, Ramanathan A, Tanabe S (2014) Methylated and unsubstituted polycyclic aromatic hydrocarbons in street dust from Vietnam and India: occurrence, distribution and in vitro toxicity evaluation. Environ Pollut 194:272–280Google Scholar
  241. Ulrich AC, Beller HR, Edwards EA (2005) Metabolites detected during biodegradation of 13C6-benzene in nitrate-reducing and methanogenic enrichment cultures. Environ Sci Technol 39:6681–6691Google Scholar
  242. US EPA (1980) Ambient water quality criteria for polynuclear aromatic hydrocarbons. Office of Water Regulation and Standards, Washington. EPA 440/5–80–069Google Scholar
  243. US EPA (1982) An exposure and risk assessment for benzo(a)pyrene and other polycyclic aromatic hydrocarbons. Vol. 1. Summary. United States Environmental Protection Agency, Washington. EPA-440/4-85-020-V1. 1982Google Scholar
  244. US EPA (2008) Polycyclic aromatic hydrocarbons (PAHs). Office of the Solid Waste, United States Environmental Protection Agency, Washington. https://archive.epa.gov/epawaste/hazard/wastemin/web/pdf/pahs.pdf. Accessed 12 Nov 2018Google Scholar
  245. Valerio F, Bottino P, Ugolini D, Cimberle MR, Tozzi GA, Frigerio A (1984) Chemical and photochemical degradation of polycyclic aromatic hydrocarbons in the atmosphere. Sci Total Environ 40:169–188Google Scholar
  246. Vázquez-Duhalt R, Ayala M, Márquez-Rocha FJ (2001) Biocatalytic chlorination of aromatic hydrocarbons by chloroperoxidase of Caldariomyces fumago. Phytochemistry 58:929–933Google Scholar
  247. Vogel TM, Grbic-Galic D (1986) Incorporation of oxygen from water into toluene and benzene during anaerobic fermentative transformation. Appl Environ Microbiol 52:200–202Google Scholar
  248. Wan R, Zhang S, Xie S (2012) Microbial community changes in aquifer sediment microcosm for anaerobic anthracene biodegradation under methanogenic condition. J Environ Sci 24:1498–1503Google Scholar
  249. Wang X-C, Zhang Y-X, Chen RF (2001) Distribution and partitioning of polycyclic aromatic hydrocarbons (PAHs) in different size fractions in sediments from Boston Harbor, United States. Mar Pollut Bull 42:1139–1149Google Scholar
  250. Wania F, Mackay D (1993) Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions. Ambio 22:10–18Google Scholar
  251. Wania F, Mackay D (1995) A global distribution model for persistent organic chemicals. Sci Total Environ 160:211–232Google Scholar
  252. Wania F, Mackay D (1996) Peer reviewed: tracking the distribution of persistent organic pollutants. Environ Sci Technol 30:390A–396AGoogle Scholar
  253. Warshawsky D, Cody T, Radike M, Reilman R, Schumann B, LaDow K, Schneider J (1995) Biotransformation of benzo[a]pyrene and other polycyclic aromatic hydrocarbons and heterocyclic analogs by several green algae and other algal species under gold and white light. Chem Biol Interact 97:131–148Google Scholar
  254. Warshawsky D, LaDow K, Schneider J (2007) Enhanced degradation of benzo[a]pyrene by Mycobacterium sp. in conjunction with green alga. Chemosphere 69:500–506Google Scholar
  255. Wawrik B et al (2012) Field and laboratory studies on the bioconversion of coal to methane in the San Juan Basin. FEMS Microbiol Ecol 81:26–42Google Scholar
  256. Wei C, Bandowe BAM, Han Y, Cao J, Zhan C, Wilcke W (2015) Polycyclic aromatic hydrocarbons (PAHs) and their derivatives (alkyl-PAHs, oxygenated-PAHs, nitrated-PAHs and azaarenes) in urban road dusts from Xi’an, Central China. Chemosphere 134:512–520Google Scholar
  257. Weiner JM, Lauck TS, Lovley DR (1998) Enhanced anaerobic benzene degradation with the addition of sulfate. Biorem J 2:159–173Google Scholar
  258. Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin WF (2016) The physiology and habitat of the last universal common ancestor. Nat Microbiol 1:16116Google Scholar
  259. Weyrauch P, Zaytsev AV, Stephan S, Kocks L, Schmitz OJ, Golding BT, Meckenstock RU (2017) Conversion of cis-2-carboxycyclohexylacetyl-CoA in the downstream pathway of anaerobic naphthalene degradation. Environ Microbiol 19:2819–2830Google Scholar
  260. White P, Claxton L (2004) Mutagens in contaminated soil: a review. Mutat Res 567:227–345Google Scholar
  261. Widdel F, Bak F (1992) Gram-negative mesophilic sulfate-reducing bacteria. In: The prokaryotes. Springer, New York, pp 3352–3378Google Scholar
  262. Wiktorska K, Misiewicz-Krzeminska I, Kasprzycka-Guttman T (2004) Polycyclic aromatic hydrocarbons: physicochemical properties, environmental appearance and impact on living organisms. Acta Pol Pharm 61(3):233–240Google Scholar
  263. Wilcke W (2000) Synopsis polycyclic aromatic hydrocarbons (PAHs) in soil – a review. J Plant Nutr Soil Sci 163:229–248Google Scholar
  264. Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the United Kingdom environment: a preliminary source inventory and budget. Environ Pollut 88:91–108Google Scholar
  265. Wilson SC, Jones KC (1993) Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): a review. Environ Pollut 81:229–249Google Scholar
  266. Wischgoll S, Taubert M, Peters F, Jehmlich N, von Bergen M, Boll M (2009) Decarboxylating and nondecarboxylating glutaryl-coenzyme a dehydrogenases in the aromatic metabolism of obligately anaerobic bacteria. J Bacteriol 191:4401–4409Google Scholar
  267. Wu RS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45Google Scholar
  268. Xu M et al (2014) Elevated nitrate enriches microbial functional genes for potential bioremediation of complexly contaminated sediments. ISME J 8:1932Google Scholar
  269. Xu M, He Z, Zhang Q, Liu J, Guo J, Sun G, Zhou J (2015) Responses of aromatic-degrading microbial communities to elevated nitrate in sediments. Environ Sci Technol 49:12422–12431Google Scholar
  270. Yan Z, Zhang Y, Wu H, Yang M, Zhang H, Hao Z, Jiang H (2017) Isolation and characterization of a bacterial strain Hydrogenophaga sp. PYR1 for anaerobic pyrene and benzo[a]pyrene biodegradation. RSC Adv 7:46690–46698Google Scholar
  271. Yang X, Ye J, Lyu L, Wu Q, Zhang R (2013) Anaerobic biodegradation of pyrene by Paracoccus denitrificans under various nitrate/nitrite-reducing conditions. Water Air Soil Pollut 224:1578Google Scholar
  272. Yu H (2002) Environmental carcinogenic polycyclic aromatic hydrocarbons: photochemistry and phototoxicity. J Environ Sci Health C 20:149–183Google Scholar
  273. Yuan SY, Chang BV (2007) Anaerobic degradation of five polycyclic aromatic hydrocarbons from river sediment in Taiwan. J Environ Sci Health B 42:63–69Google Scholar
  274. Zhang Y, Tao S (2009) Global atmospheric emission inventory of polycyclic aromatic hydrocarbons (PAHs) for 2004. Atmos Environ 43:812–819Google Scholar
  275. Zhang X, Young LY (1997) Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol 63:4759–4764Google Scholar
  276. Zhang X, Sullivan ER, Young LY (2000) Evidence for aromatic ring reduction in the biodegradation pathway of carboxylated naphthalene by a sulfate reducing consortium. Biodegradation 11:117–124Google Scholar
  277. Zhang S, Wang Q, Xie S (2012a) Molecular characterization of phenanthrene-degrading methanogenic communities in leachate-contaminated aquifer sediment. Int J Environ Sci Technol 9:705–712Google Scholar
  278. Zhang S, Wang Q, Xie S (2012b) Stable isotope probing identifies anthracene degraders under methanogenic conditions. Biodegradation 23:221–230Google Scholar
  279. Zhang T, Tremblay P-L, Chaurasia AK, Smith JA, Bain TS, Lovley DR (2013) Anaerobic benzene oxidation via phenol in Geobacter metallireducens. Appl Environ Microbiol 79:7800–7806Google Scholar
  280. Zhou Z, Yao Y, Wang M, Zuo X (2017) Co-effects of pyrene and nitrate on the activity and abundance of soil denitrifiers under anaerobic condition. Arch Microbiol 199:1091–1101Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Kartik Dhar
    • 1
    • 2
  • Suresh R. Subashchandrabose
    • 1
  • Kadiyala Venkateswarlu
    • 3
  • Kannan Krishnan
    • 1
  • Mallavarapu Megharaj
    • 1
    Email author
  1. 1.Global Centre for Environmental Remediation (GCER), Faculty of ScienceThe University of NewcastleCallaghanAustralia
  2. 2.Department of MicrobiologyUniversity of ChittagongChittagongBangladesh
  3. 3.Formerly Department of MicrobiologySri Krishnadevaraya UniversityAnantapuramuIndia

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