InTechOpen uses cookies to offer you the best online experience. By continuing to use our site, you agree to our Privacy Policy.

Environmental Sciences » "Biodegradation and Bioremediation of Polluted Systems - New Advances and Technologies", book edited by Rolando Chamy, Francisca Rosenkranz and Lorena Soler, ISBN 978-953-51-2238-8, Published: December 17, 2015 under CC BY 3.0 license. © The Author(s).

Chapter 6

Biodegradation of Aromatic Compounds

By Mehdi Hassanshahian, Moslem Abarian and Simone Cappello
DOI: 10.5772/60894

Article top


Structures of U.S. EPA’s 16 priority pollutant PAH [1].
Figure 1. Structures of U.S. EPA’s 16 priority pollutant PAH [1].
Diagram of the transfer of PAHs in the environment [24].
Figure 2. Diagram of the transfer of PAHs in the environment [24].
Seeps, oil spills from boats or platforms, and produced water discharge from oil- and gass-producing installations such as the one shown. PAHs in produced water and oil seeps represent a chronic release to the marine enviroments [37]
Figure 3. Seeps, oil spills from boats or platforms, and produced water discharge from oil- and gass-producing installations such as the one shown. PAHs in produced water and oil seeps represent a chronic release to the marine enviroments [37]
Biodegradation of aromatic hydrocarbons: metabolism begins with the activity of a mono-oxygenase or a dioxygenase [36].
Figure 4. Biodegradation of aromatic hydrocarbons: metabolism begins with the activity of a mono-oxygenase or a dioxygenase [36].
Proposed anaerobic biotransformation pathway of phenanthrene by sulfate-reducing bacteria [38].
Figure 5. Proposed anaerobic biotransformation pathway of phenanthrene by sulfate-reducing bacteria [38].
Proposed pathway for microbial catabolism of polycyclic aromatic hydrocarbons [39].
Figure 6. Proposed pathway for microbial catabolism of polycyclic aromatic hydrocarbons [39].

Biodegradation of Aromatic Compounds

Mehdi Hassanshahian1, Moslem Abarian1 and Simone Cappello2

1. Introduction

Polycyclic aromatic hydrocarbons (PAHs) are the major group of marine contaminants that are made of two or more benzene rings. Polycyclic aromatic hydrocarbons (PAHs) are one of the major categories of pollutants entering the marine environment and finally accumulating in the sediments. Their occurrence raises major concerns for human health, especially during coastal activities (bathing waters, aquaculture, etc.), having combined adverse effects still largely [1]. The solubility of these compounds in the seawater is low, and they tend to be bounded to suspended organic matter in the water column and finally accumulate in the marine sediment [2, 3]. Many researchers have experimentally worked on the biodegradation of PAHs, which involves the use of specific microorganisms, specific reducing culture, metabolic pathways, bioavailability and disappearance, growth of the microbes under aerated and unaerated conditions, pH variation, and kinetics of biodegradation [4]. The bacteria were capable of growing on various hydrocarbons like diesel, petrol, lubricating oil, toluene, naphthalene, and kerosene. The tests were conducted to detect the biodegradation of diesel, by amino-oxygenase biodegradation pathway, and it was observed that diesel was degraded within 12 hours [5].

2. Polycyclic Aromatic Hydrocarbons (PAHs)

Polycyclic aromatic hydrocarbons (PAHs) are a group of approximately 10, 000 compounds that are atmospheric, water, and soil pollutants. They are organic contaminants that are formed from the incomplete combustion of a variety of organic compounds. The structure of a PAH consists of molecules containing two or more fused six-carbon atom aromatic rings; only hydrogen and carbon are present in the molecules. There are 18 PAHs considered by the Agency for Toxic Substances and Disease Registry that have adverse health effects: acenaphthene, acenaphthylene, anthracene, benzo[a]anthracene, benzo[a]pyrene, benzo[e]-pyrene, benzo[b] fluoranthene, benzo[ghi]perylene, benzo[j]fluoranthene, benzo[k]fluoranthene, chrysene, coronene, dibenz(a, h)anthracene, fluoranthene, fluorene, indeno(1, 2, 3-cd)pyrene, phenanthrene, and pyrene[6, 7]. Figure [1] shows some PAHs.


Figure 1.

Structures of U.S. EPA’s 16 priority pollutant PAH [1].

2.1. Phenanthrene (Phe), pyrene (Pyr), and benzo[e]pyrene (BeP)

The most PAHs in oil products have two and three fused benzene rings with one to four carbon atom alkyl group substitutions. Naphthalene, the two-benzene-ring PAH, often present in significant amounts in petroleum, is relatively volatile, soluble, and degradable. Therefore, naphthalene in weathered oil from an offshore spill may not be available when the contaminated water reaches coastal environments; on the other hand, higher molecular weight species such as phenanthrene (three-benzene-ring PAH), pyrene (four-benzene-ring PAH), and benzo[e]pyrene (five-benzene-ring PAH) can be found in weathered crude oils reaching coastal wetlands. The higher the number of benzene-rings the PAH has, the higher the molecular weight, but the lower the solubility in water [17, 29].

3. Sources of PAHs

The sources of PAHs in a marine environment could include volcanoes, natural fires, fossil fuel fired power generation, combustion engines, municipal discharges, oil pipeline spills, oil fields, offshore drilling platforms, natural oil seeps, and shipping accidents [6]. The sources of PAH are illustrated in Figure 2.


Figure 2.

Diagram of the transfer of PAHs in the environment [24].

3.1. PAHs in water

The main sources of PAHs in water bodies are atmospheric particulate matter deposition, runoff of polluted ground sources, and pollution of river and lakes by industrial effluents, municipal wastewater discharge, and oil spills [14]. Since PAHs have low solubility and tend to adsorb to particulate matter, they are usually found in low concentrations in water bodies. Some PAH concentrations that have been measured in water include marine waters with levels of nondetected to 11 g L-1 wastewater in North American and European municipalities with levels of <1 to 625 g L-1 and urban runoff in the U.S. with levels of <0.05 to 560 g L-1 [14, 15].

3.2. Sources of PAHs in coastal environments and marine

PAHs in coastal environments can come from many sources naturally as well as through anthropogenic activity. They adsorb and tend to stay longer in sediment due to their hydrophobicity (low solubility and high octanol-water partition coefficient). The main sources of PAHs in a marine ecosystem are atmospheric deposition, river runoff, domestic and industrial wastewater, and direct spillage of oil or petroleum products [16]. Figure 3 shows the source of PAH in the marine environment.


Figure 3.

Seeps, oil spills from boats or platforms, and produced water discharge from oil- and gass-producing installations such as the one shown. PAHs in produced water and oil seeps represent a chronic release to the marine enviroments [37]

4. PAHs biodegradation

PAHs are toxic to marine species and to the environment. As they are absorbed into soil/sediment, many hydrophobic PAHs in soil-water interfaces undergo some physical, chemical, and biological degradation, but biodegradation is the most effective process. Microorganisms utilize only dissolved substrates; and the utilization rates of PAH degradation products are related to sorption/desorption rates of PAHs to and from soil. Since biodegradation is assumed to be the main reaction in PAH decay in soil, microorganisms require some nutrients to survive and to function. The nutrients in shortest supply are usually nitrogen (N), phosphorus (P), or both, while the supply of K, S, Mg, Ca, Fe, and micronutrient elements is nearly always greater than the demand [16]. Some nutrients can be added to wetland soil and water to enhance the degradation of organic material. The capacity of different wetland soil to retain nutrients may be different. Therefore, it is necessary to investigate PAH degradations in the subtidal and the intertidal wetland soil with the addition of nutrients.

Specific characteristics of coastal wetland ecosystems that make them suitable for PAH biodegradation processes are the large quantity of water, the oxic and anoxic soil for the breakdown of organic matter, and the supporting highly productive, tall emergent vegetation. Some organic compounds degrade favorably under aerobic conditions, such as naphthalene; other compounds degrade favorably under anaerobic conditions, such as DDT; and some others degrade favorably under moderately anaerobic conditions, such as PCBs. Understanding of PAHs degradation pathways and kinetics provides guidance for the selection of effective methods and technology to remediate a contaminated site [18]. The schematic biodegradation of PAHs is described in Figure 4.


Figure 4.

Biodegradation of aromatic hydrocarbons: metabolism begins with the activity of a mono-oxygenase or a dioxygenase [36].

4.1. Properties PAHs in biodegradation

Pure compounds of PAHs with higher molecular weights are more resistant to biotransformation and pure compounds of PAHs with lower molecular weights transform more rapidly [30]. However, the presence of one PAH can decrease the biodegradation of other PAHs. With the simultaneous presence of phenanthrene, acenaphthene, fluorine, anthracene, pyrene, and benzo[a]pyrene, the biodegradation was decreased for phenanthrene and acenaphtene but was enhanced for fluorine, anthracene, and pyrene (while biodegradation of benzo[a]pyrene did not occur within a 12-day incubation period [31]. There are thousands of PAH compounds in the environment, but in practice, PAH analysis is restricted to the determination of 6 to 16 compounds. Individual PAHs differ substantially in their physical and chemical properties. Generally, the high molecular weight compounds (≥ 4 aromatic rings) are less water soluble, less volatile, and more lipophilic than lower molecular weight ones. The best known model compound from this group is highly carcinogenic benzo[a]pyrene (BaP). PAHs are listed by the U.S. Environmental Protection Agency and the European Commission as priority pollutants [32].

4.2. PAH-degrading bacteria

PAH degradation has been known for many years to occur in marine sediments. Previous results indicate that culturable hydrocarbon-degrading and PAH-degrading populations are widely distributed and can be enriched from sites of contamination in marine environments [7, 8, 9, 10]. However, other studies indicate that high levels of PAH can be toxic to marine bacteria [11, 12, 13]. Therefore, highly contaminated sites might be inhibitory to PAH-degrading bacteria and other microorganisms.

4.3. Community from the Surface Microlayer (SML) in an estuarine

The sea surface microlayer (SML) represents the interface between the atmosphere and the hydrosphere. Organisms within the SML are known as neuston, and the community of bacteria present within this neuston layer is named bacterioneuston. Acinetobacter and Rhizobium were also found among the PAH-degrading isolates retrieved from the SML. Many environmental strains of Acinetobacter with hydrocarbon-degrading capacities have been isolated in terrestrial and marine environments [19]. The subclass gamma-Proteobacteria was relatively more abundant in bacterioneuston (SML) than in bacterioplankton. The gamma-Proteobacteria subclass includes major PAH-degrading genera, such as Alcanivorax, Cycloclasticus, Pseudomonas, Oleiphilus, Oleispira, and Thalassolituus [20, 21].

4.4. PAH-degrading bacteria in coastal sediment

It is well known that bacterial degradation plays an important role in PAHs removal from the marine environment. Many PAH-degrading bacteria have been found in coastal sediments, including bacteria of Cycloclasticus, Marinobacter, Pseudoalteromonas, Marinomonas, Sphingomonas, Vibrio, and Halomonas. However, knowledge about deep-sea environments is relatively less. In previous studies on the deep-sea sediments of Atlantic Ocean and Pacific Ocean, Cycloclasticus was the most important bacterium, in addition to Alteromonas and Novosphingobium [22, 23].

5. Toxicity and the effects of PAHs

PAHs reveal their toxicity following biotransformation to toxic metabolites, which can be bond covalently to cellular macromolecules such as DNA, RNA, and protein. The major PAH-metabolizing enzymes are cytochrome P450 mono-oxygenases, epoxide hydrolase, and several conjugating enzymes [25]. Highly carcinogenic 7, 8- and 9, 10-dihydrodiols are the major PAH metabolites produced by fish microsomes. The metabolites of PAH are mainly conjugated with glucuronic acid. Most conjugates are water-soluble organic anions and are rapidly excreted mostly via the gallbladder or in urine PAHs with high molecular weight, which are not acutely toxic to fish. However, in the presence of solar ultraviolet radiation, many of them are acutely toxic. Exposure to PAHs causes the suppression of the immune system. A decreased number of melano-macrophage centers in the liver and suppression of proliferative responses of T-lymphocytes [26, 27, 28].

6. Anaerobic biodegradation PAHs

The anaerobic degradation of aromatic hydrocarbons is often presumed to be slow and of minor ecological significance. However, anaerobic biotransformation may play a key role in the transformation of aromatic and PAH compounds when oxygen demand exceeds supply in natural environments. As shown in Figure 5, under such conditions, anoxic or anaerobic degradation mediated by denitrifying or sulfate-reducing bacteria can become a key pathway for the cleanup of contaminated sites [33]. The isolation of denitrifying and sulfate-reducing organisms capable of degrading toluene has led to the elucidation of several biodegradation pathways and phylogenetic relationships between bacterial strains. The isolation of denitrifying and sulfate-reducing organisms capable of degrading toluene has led to the elucidation of several biodegradation pathways and phylogenetic relationships between bacterial strains [34, 35].


Figure 5.

Proposed anaerobic biotransformation pathway of phenanthrene by sulfate-reducing bacteria [38].

7. Aerobic biodegradation

During aerobic degradation by bacteria, PAHs are oxidized to cis-dihydrodiols through the incorporation of an oxygen molecule into the PAH. As shown in Figure 6, the cis-dihydrodiols are further oxidized to aromatic dihydroxy compounds (catechols), and then PAH rings are cleaved with intracellular dioxygenases. The oxidation of unsubstituted PAHs with very high thermodynamic stability often results in PAH compounds that are less stable than the parent compounds and more susceptible to cleavage [40, 41, 42]. Oxygenase production by bacteria can be increased using biostimulants; for example, salicylic acid is a known inducer of naphthalene dioxygenase. Linoleic acid is a powerful stimulant of pyrene and benzo[a]pyrene degradation by gram-positive bacteria. The addition of humic substances also greatly enhances the microbial degradation of PAHs [43].


Figure 6.

Proposed pathway for microbial catabolism of polycyclic aromatic hydrocarbons [39].

8. Biodegradation of benzo[a]pyrene by marine denitrifying bacteria

Benzo[a]pyrene (BaP) is one of the high molecular weight, 5 ring-PAHs and is listed as one of the priority pollutants classified as a carcinogen by the U.S. Environmental Protection Agency and the Agency for Toxic Substances and Disease Registry. BaP is ranked number 9 on the priority list of 275 substances. The toxicity of BaP is of high concern because of its ability to accumulate in animal tissues, to cause cancer and hormone disruption, and to affect reproduction. Moreover, BaP was found to depress immune function [44, 45-47]. The principal natural sources of BaP are forest fires, volcanic eruption, pest fires, and burning of crude oil. Anthropogenic sources include the incomplete combustion of coal, oil, gas, wood, rubbish, and other organic substances, incinerator, vehicle exhausts, and cigarette [48]. BaP derived from gasoline automobile accounted for 98% [48, 49]. The natural presence of PAHs in the environment allows many microorganisms to adapt to exploit this naturally occurring as the potential growth substrate. Thus, many bacterial, fungal, and algal strains have been shown to utilize wide varieties of PAHs containing from three to five aromatic rings [50]. The application of microorganisms for bioremediation of PAH-contaminated environment seems to be an attractive technology because they are more specific, effective, economic, and environmental friendly. Biodegradation in marine environment was also described attractively [50, 51]. Denitrification is an important major process; denitrifying bacteria responses to environmental conditions by cycling nitrogen gas back to the atmosphere. These denitrifying bacteria utilize nitrate (NO3-), nitrite (NO2-), nitric oxide (NO), and nitrous oxide (N2O) as terminal electron acceptors in anaerobic respiration. The denitrifying bacteria isolated from marine sediment were Bacillus subtilis in majority. B. subtilis have the ability to degrade benzo[a]pyrene with a complete degradation efficiency of the initial amount of 200 mg/l supplied over 45 days of incubation at 30°C [52, 53]. B. subtilis successfully biodegraded benzo[a]pyrene but failed to increased biomass production [54, 55].


1 - Gustafsson, O., N. Nilsson and T.D. Bucheli, 2001. Dynamic colloid-water partitioning of pyrene though a coastal Baltic Spring Bloom. Environmental Science and Technology, 35: 4001-4006.
2 - Baumard, P., H. Buzinski, Q. Michon, P. Garrigues and J. Burgeot Tand Bellocq, 1998. Origin and Bioavailability of PAHs in the Mediterranean Sea from Mussel and Sediment Records. Estuarin Coastal.
3 - Pothuluri, J.V. and C.E. Cerniglia. Current aspects on polycyclic aromatic hydrocarbon degradation processes. In: Sikdar, S.K. and Irvine, R.L., eds. Bioremediation: Principles and Practice Volume III. Lancaster USA: Technomic Publishing Company, Inc., 1998. pp. 461-520.
4 - Masih, A. and A. Taneja, 2006. Polycyclic aromatic hydrocarbons (PAHs) concentrations and related carcinogenic potencies in soil at a semi-arid region of India. Chemosphere, 65: 449-456.
5 - Geetha, S.J., S.J. Joshi and S, Kathrotiya, 2013. Isolation and characterization of hydrocarbon degrading bacterial isolate from oil contaminated sites. APCBEE Procedia, 5: 237-241.
6 - Kennish, M.J., 1996. Practical Handbook of Estuarine and Marine Pollution. CRC Press Inc., Boca Raton, FL, 524 pp.
7 - Foght, J.M., P.M. Fedorak and D.W.S. Westlake, 1990. Mineralization of 14C-hexadecane and 14C-phenanthrene in crude oil: specificity among bacterial isolates. Canadian Journal of Microbiology, 36(3): 169-175.
8 - Roubal, G. and R.M. Atlas, 1978. Distribution of hydrocarbon-utilizing microorganisms and hydrocarbon biodegradation potentials in Alaskan continental shelf areas. Applied and Environmental Microbiology, 35: 897-905.
9 - Shiaris, M.P. and J.J. Cooney, 1983. Replica plating method for estimating phenanthrene-utilizing and phenanthrene-cometabolizing microorganisms. Applied and Environmental Microbiology, 45: 706-710.
10 - West, P.A., G.C. Okpokwasili, P.R. Brayton, D.J. Grimes and R.R. Colwell, 1984. Numerical taxonomy of phenanthrene-degrading bacteria isolated from Chesapeake Bay. Applied and Environmental Microbiology, 48: 988-993.
11 - Calder, J.A. and J.H. Lader, 1976. Effect of dissolved aromatic hydrocarbons on the growth of marine bacteria in batch culture. Applied and Environmental Microbiology, 32: 95-101.
12 - Sikkema, J., J.A.M. de Bont and B. Poolman, 1995. Mechanisms of membrane toxicity of hydrocarbons. Applied and Environmental Microbiology, 59: 201-222.
13 - Tuveson, R.W., J. Kagan, M.A. Shaw, G.M. Moresco, E.M.V. Behne, H. Pu, M. Basin and R. Santus, 1987. Phototoxic effects of fluoranthene, a polycyclic aromatic hydrocarbon, on bacterial species. Environmental and Molecular Mutagenesis, 10: 245-261.
14 - Latimer, J. and J. Zheng, 2003. The sources, transport, and fate of PAH in the marine environment. pp. 9-31. In: P.E.T. Douben, ed. PAHs: An Ecotoxicological Perspective.
15 - Dabestani, R. and I. Ivanov, 1999. A compilation of physical, spectroscopic and photophysical properties of poly aromatic hydrocarbons. Photochemistry and Photobiology, 70: 10-34.
16 - Alexander, M., 1999. Biodegradation and Bioremediation, 2nd ed. Ithaca, NY: Academic Press, 453 pp.
17 - ATSDR, 2005. Toxic substances portal—polycyclic aromatic hydrocarbons (PAHs). Agency for Toxic Substances and Disease Registry U.S. Department of Health and Human Services, Public Health Service. Atlanta, GA.
18 - Reddy, K.R. and R.D. DeLaune, 2008. Biogeochemistry of Wetlands: Science and Applications. Taylor & Francis Group, 774 pp.
19 - Karolien, V., R. Annemie, W. Pierre, M. René and S. Dirk, 2004. Acinetobacter diversity in environmental samples assessed by 16S rRNA gene PCR-DGGE fingerprinting. FEMS Microbiology Ecology, 50: 37-50.
20 - Watanabe, K., 2001. Microorganisms relevant to bioremediation. Current Opinion in Biotechnology, 12: 237-241.
21 - Franklin, M.P., I.R. McDonald, D.G. Bourne, N.J. Owens, R.C. Upstill-Goddard and J.C. Murrell, 2005. Bacterial diversity in the bacterioneuston (sea surface microlayer): the bacterioneuston through the looking glass. Environmental Microbiology, 7: 723-736.
22 - Dong, C., X. Bai, H. Sheng, L. Jiao, H. Zhou and Z. Shao, 2014. Distribution of PAHs and the PAH-degrading bacteria in the deep-sea sediments of the high-latitude Arctic Ocean. Biogeosciences Discussion, 11: 13985-14021.
23 - Cui, Z., Lai, Q., Dong, C., and Shao, Z, 2008. Biodiversity of polycyclic aromatic hydrocarbondegrading bacteria from deep sea sediments of the Middle Atlantic Ridge, Environmental Microbiology, 30 10: 2138-2149,.
24 - Abbey, F., Wick Nicholas, W., Haus Beshr, F., Sukkariyah, Kathryn, C and Haering Lee Daniels, W.2011. Remediation of PAH contaminated soils and sediments a literature review. Virginia Polytechnic Institute and State University Department of Crop and Soil Environmental Sciences. 1-102.
25 - Masfaraud, J.F., Pfohl-Leszkowic, A., Malaveille, C., Keith, G., and Monod, G, 1992. 7-Ethylresorufin O-Deethylase Activity and level of DNA-Adduct in Trout Treated with Benzo(a)pyren. Marine Environmental Research. 34:351-354.
26 - Faisal, M., Weeks, B.A., Vogelbien, W.K and Huggett, R.J, 1991. Evidence of aberration of the natural cytotoxic cell activity in Fandalus heteroclitus (Pisces:Cyprinodontidae) from the Elizabeth River, Virginia. Veterinary Immunology and Immunopathology, 29(3-4): 339-351.
27 - Myers, M.S., Olson, O.P., Johnson, L.L, Stehr, C.S, Hom, T. and Varanasi, U.1992. Hepatic lesion other than neoplasms subadult flatfish from Puget Sound Vashington: Relationship with indices of contaminated exposure. Marine Environmental Research, 34: 45-51.
28 - Maccubbin, A.E, 1994. DNA adduct analysis in fish: laboratory and field studies. In: Malins, D.C. and Ostrander, G.K., eds. Aquatic Toxicology: Molecular, Biochemical, and Cellular Perspective. USA: CRC press, pp. 267-294.
29 - Overton, E.B., W.D. Sharp and P. Roberts, 1994. Toxicity of petroleum. In: Cockerham, L.G. and Shane, B.S., eds. Basic Environmental Toxicology. Boca Raton, FL: CRC Press, pp. 133-156.
30 - Park, K.S., R.C. Sims and R. Dupont, 1990. Transformation of PAHs in soil systems. Journal of Environmental Engineering (ASCE), 116: 623-640.
31 - Yuan, S.Y., J.S. Chang, J.H. Yen, B.V. Chang, 2001. Biodegradation of phenanthrene in river sediment. Chemosphere, 43: 273-278.
32 - Bakowski, W. and D. Bodzek, 1988. WielopierScieniowe weglowodory aromatyczne w naturalnym srodowisku czlowieka—pochodzenie, wystepowanie, toksycznosc, oszacowanie emisjiw Polsce. Arch Ochr Srodow, 3-4: 195.
33 - Edwards, E.A., L.E. Wills and D. Grbic-Galic, 1991. Anaerobic degradation of toluene and xylene—evidence for sulfate as the terminal electron acceptor. In: Hinchee, R.E. and Olfenbuttel, R., eds. In Situ Bioreclamation: Applications and Investigations for Hydrocarbon and Contaminated Site Remediation. Stoneham, MS: Butterworth-Heinemann, 463-471 pp.
34 - Biegert, T., G. Fuchs and J. Heider, 1996. Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumerate. European Journal of Biochemistry, 238: 661-668.
35 - Rockne, K.J. and S.E. Strand, 1998. Biodegradation of bicyclic and polycyclic aromatic hydrocarbons in anaerobic enrichments. Environmental Science and Technology, 32: 3962-3967.
36 - Alloway, B.J. and D.C. Ayres, 1993.Organic pollutants. In: Chemical Principles of Environmental Pollution, 1st ed. India: Chapman and Hall.
37 - Pampanin, D.M. and O. Sydnes, 2013. Polycyclic aromatic hydrocarbons a constituent of petroleum: presence and influence in the aquatic environment. Intech, 1-36.
38 - Tsai, J.-C., M. Kumar and J.-G. Lin, 2009. Anaerobic biotransformation of fluorene and phenanthrene by sulfate-reducing bacteria and identification of biotransformation pathway. Journal of Hazardous Materials, 164 (2-3): 847-855.
39 - C.E. Cerniglia, 1992. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation, 3: 351-368.
40 - Alexander, M., 1999. Biodegradation and Bioremediation, 2nd ed. San Diego, CA: Academic Press.
41 - Ghanavati, H., G. Emtiazi and M. Hassanshahian, 2008. Synergism effects of phenol degrading yeast and ammonia oxidizing bacteria for nitrification in coke wastewater of Esfahan steel company. Waste Management and Research, 26 (2): 203-208.
42 - Hasanshahian, M. and G. Emtiazi, 2008. Investigation of alkane biodegradation using the microtiter plate method and correlation between biofilm formation, biosurfactant production and crude oil biodegradation. International Biodeterioration and Biodegradation, 62: 170-178.
43 - Hassanshahian, M., G. Emtiazi, R. Kermanshahi and S. Cappello, 2010. Comparison of oil degrading microbial communities in sediments from the Persian Gulf and Caspian Sea. Soil and Sediment Contamination, 19 (3): 277-291.
44 - Hassanshahian, M., H. Tebyanian and S. Cappello, 2012a. Isolation and characterization of two crude-oil degrading yeast strains, Yarrowia lipolytica PG-20 and PG-32 from Persian Gulf. Marine Pollution Bulletin, 64: 1386-1391.
45 - Hassanshahian, M., G. Emtiazi and S. Cappello, 2012b. Isolation and characterization of crude-oil-degrading bacteria from the Persian Gulf and the Caspian Sea. Marine Pollution Bulletin, 64: 7-12.
46 - Hassanshahian, M., M. Ahmadinejad, H. Tebyanian and A. Kariminik, 2013. Isolation and characterization of alkane degrading bacteria from petroleum reservoir waste water in Iran (Kerman and Tehran provenances). Marine Pollution Bulletin, 73: 300-305.
47 - Hassanshahian, M., G. Emtiazi, G. Caruso, S. Cappello, 2014a. Bioremediation (bioaugmentation/biostimulation) trials of oil polluted seawater: a mesocosm simulation study. Marine Environmental Research, 95: 28-38.
48 - Hassanshahian, M., M.S. Zeynalipour and F.Hosseinzadeh Musa, 2014b. Isolation and characterization of crude oil degrading bacteria from the Persian Gulf (Khorramshahr provenance). Marine Pollution Bulletin, 82: 39-44.
49 - Hassanshahian, M., M.M. Yakimov, R. Denaro, M. Genovese and S. Cappello, 2014c. Using real-time PCR to assess changes in the crude oil degrading microbial community in contaminated seawater mesocosms. International Biodeterioration and Biodegradation, 93: 241-248.
50 - Tebyanian, H., M. Hassanshahian and A. Kariminik, 2013. hexadecane-degradation by Teskumurella and Stenotrophomonas strains isolated from hydrocarbon contaminated soils. Jundishapur Journal of Microbiology, 26 (7): e9182.
51 - Hassanshahian, M. and M.M. Yaghoobi, 2014. Cloning and gene expression of cytochrome P450 gene from Alcanivorax borkumensis Bacterium. International Journal of Advanced Biological and Biomedical Research, 2(1): 76-85.
52 - Amini Boroujeni, N., M. Hassanshahian and M.R. Khoshrou, 2014. Isolation and characterization of phenol degrading bacteria from Persian Gulf. International Journal of Advanced Biological and Biomedical Research, 2(2): 408-416.
53 - Hassanshahian, M., 2014. The effects of crude oil on marine microbial communities in sediments from the Persian Gulf and the Caspian Sea: a microcosm experiment. International Journal of Advanced Biological and Biomedical Research, 2(1): 1-17.
54 - Hassanshahian, M. and S. Cappello, 2013. Crude oil biodegradation in the marine environments. In: Biodegradation—Engineering and Technology (Chapter 5). InTech Open Science, 101-135.
55 - R.D. Hunter, S.I.N. Ekunwe, D.E Dodor, H-M Hwang and Ekunwe, 2005. Bacillus subtilis is a potential degrader of pyrene and benzo(a)pyrene. International Journal of Environmental Research and Public Health, 2(2): 267-271.