new, extremely halotolerant, hydrocarbon-degrading
marine bacterium. Int J Syst Evol Microbiol 42, 568–576.
Genovese, M., Crisafi, F., Denaro, R., Cappello, S., Russo, D.,
Calogero, R., Santisi, S., Catalfamo, M. et al. (2014)
Effective bioremediation strategy for rapid in situ cleanup
of anoxic marine sediments in mesocosm oil spill
simulation. Front Microbiol 5, 162.
Gentile, G., Bonsignore, M., Santisi, S., Catalfamo, M.,
Giuliano, L., Genovese, L., Yakimov, M.M., Denaro, R.
et al. (2016) Biodegradation potentiality of psychrophilic
bacterial strain Oleispira antarctica RB-8T. Marine Poll
Bull 105, 125–130.
GESAMP. (1993) Impact of oil and related chemicals and
wastes on the marine environment. Rep Stud GESAMP.
Golyshin, P.N., Chernikova, T.N., Abraham, W.R., L€ unsdorf,
H., Timmis, K.N. and Yakimov, M.M. (2002)
Oleiphilaceae fam. nov., to include Oleiphilus messinensis
gen. nov., sp. nov., a novel marine bacterium that
obligately utilizes hydrocarbons. Int J Syst Evol Microbiol
52, 901–911.
Goodfellow, M. and Maldonado, L.A. (2006) The families
dietziaceae, gordoniaceae, nocardiaceae and
tsukamurellaceae. In The prokaryotes ed. Dworkin, M.,
Falkow, S., Rosenberg, E., Schleifer, K.H. and
Stackebrandt, E. pp. 843–888. New York, NY: Springer.
Hara, A., Syutsubo, K. and Harayama, S. (2003) Alcanivorax
which prevails in oil-contaminated seawater exhibits broad
substrate specificity for alkane degradation. Environ
Microbiol 5, 746–753.
Hara, A., Baik, S.H., Syutsubo, K., Misawa, N., Smits, T.H.,
van Beilen, J.B. and Harayama, S. (2004) Cloning and
functional analysis of alkB genes in Alcanivorax
borkumensis SK2. Environ Microbiol 6, 191–197.
Harayama, S., Kasai, Y. and Hara, A. (2004) Microbial
communities in oil-contaminated seawater. Curr Opin
Biotechnol 15, 205–214.
Hassanshahian, M., Emtiazi, G. and Cappello, S. (2012)
Isolation and characterization of crude-oil-degrading
bacteria from the Persian Gulf and the Caspian Sea.
Marine Poll Bull 64, 7–12.
Hedlund, B.P., Geiselbrecht, A.D., Bair, T.J. and Staley, J.T.
(1999) Polycyclic aromatic hydrocarbon degradation by a
new marine bacterium, Neptunomonas naphthovorans gen.
nov., sp. nov. Appl Environ Microbiol 65, 251–259.
Hendrickx, B., Junca, H., Vosahlova, J., Lindner, A., R€ uegg, I.,
Bucheli-Witschel, M., Faber, F., Egli, T. et al. (2006)
Alternative primer sets for PCR detection of genotypes
involved in bacterial aerobic BTEX degradation:
distribution of the genes in BTEX degrading isolates and
in subsurface soils of a BTEX contaminated industrial site.
J Microbiol Methods 64, 250–265.
Kasai, Y., Kishira, H., Sasaki, T., Syutsubo, K., Watanabe, K.
and Harayama, S. (2002) Predominant growth of
Alcanivorax strains in oil-contaminated and nutrientsupplemented sea water. Environ Microbiol 4, 141–147.
Kloos, K., Munch, J.C. and Schloter, M. (2006) A new method
for the detection of alkane-monooxygenase homologous
genes (alkB) in soils based on PCR-hybridization. J
Microbiol Methods 66, 486–496.
Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic acid
techniques in bacterial systematics ed. Stackebrandt, E. and
Goodfellow, M. pp. 115–175. New York: Wiley.
Lo Piccolo, L., De Pasquale, C., Fodale, R., Puglia, A.M. and
Quatrini, P. (2011) Involvement of an alkane hydroxylase
system of Gordonia sp. strain SoCg in degradation of
solid n-alkanes. Appl Environ Microbiol 77, 1204–1213.
Mahjoubi, M., Jaouani, A., Guesmi, A., Amor, S.B., Jouini, A.,
Cherif, H., Najjari, A., Boudabous, A. et al. (2013)
Hydrocarbonoclastic bacteria isolated from petroleum
contaminated sites in Tunisia: isolation, identification and
characterization of the biotechnological potential. N
Biotechnol 30, 723–733.
Malik, Z. and Ahmed, S. (2012) Degradation of petroleum
hydrocarbons by oil field isolated bacterial consortium.
Afr J Biotechnol 11, 650–658.
McKew, B.A., Coulon, F., Yakimov, M.M., Denaro, R.,
Genovese, M., Smith, C.J., Osborn, A.M., Timmis, K.N.
et al. (2007) Efficacy of intervention strategies for
bioremediation of crude oil in marine systems and effects
on indigenous hydrocarbonoclastic bacteria. Environ
Microbiol 9, 1562–1571.
M’rassi, A.G., Bensalah, F., Gury, J. and Duran, R. (2015)
Isolation and characterization of different bacterial strains
for bioremediation of n-alkanes and polycyclic aromatic
hydrocarbons. Environ Sci Poll Res 22, 15332–15346.
Muyzer, G., De Waal, E.C. and Uitterlinden, A.G. (1993)
Profiling of complex microbial populations by denaturing
gradient gel electrophoresis analysis of polymerase chain
reaction-amplified genes coding for 16S rRNA. Appl
Environ Microbiol 59, 695–700.
Porter, K.G. and Feig, Y.S. (1980) The use of DAPI for
identifying and counting aquatic microflora 1. Limnol
Oceanogr 25, 943–948.
Quatrini, P., Scaglione, G., De Pasquale, C., Riela, S. and
Puglia, A.M. (2008) Isolation of Gram-positive nalkane degraders from a hydrocarbon-contaminated
Mediterranean shoreline. J Appl Microbiol 104, 251–
259.
Rajaei, S., Seyedi, S.M., Raiesi, F., Shiran, B. and Raheb, J.
(2013) Characterization and potentials of indigenous oildegrading bacteria inhabiting the rhizosphere of wild oat
(Avena fatua L.) in South West of Iran. Iran J
Biotechnol 11, 32–40.
R€ oling, W.F., Milner, M.G., Jones, D.M., Lee, K., Daniel, F.,
Swannell, R.J. and Head, I.M. (2002) Robust hydrocarbon
degradation and dynamics of bacterial communities
during nutrient-enhanced oil spill bioremediation. Appl
Environ Microbiol 68, 5537–5548.
Santisi, S., Cappello, S., Catalfamo, M., Mancini, G.,
Hassanshahian, M., Genovese, L., Giuliano, L. and
Journal of Applied Microbiology 126, 780--795 © 2018 The Society for Applied Microbiology
794
The use of oil-degrading bacteria as an alternative for environmental remediation (bioremediation)
N. Djahnit et al.
marine bacterium. Int J Syst Evol Microbiol 42, 568–576.
Genovese, M., Crisafi, F., Denaro, R., Cappello, S., Russo, D.,
Calogero, R., Santisi, S., Catalfamo, M. et al. (2014)
Effective bioremediation strategy for rapid in situ cleanup
of anoxic marine sediments in mesocosm oil spill
simulation. Front Microbiol 5, 162.
Gentile, G., Bonsignore, M., Santisi, S., Catalfamo, M.,
Giuliano, L., Genovese, L., Yakimov, M.M., Denaro, R.
et al. (2016) Biodegradation potentiality of psychrophilic
bacterial strain Oleispira antarctica RB-8T. Marine Poll
Bull 105, 125–130.
GESAMP. (1993) Impact of oil and related chemicals and
wastes on the marine environment. Rep Stud GESAMP.
Golyshin, P.N., Chernikova, T.N., Abraham, W.R., L€ unsdorf,
H., Timmis, K.N. and Yakimov, M.M. (2002)
Oleiphilaceae fam. nov., to include Oleiphilus messinensis
gen. nov., sp. nov., a novel marine bacterium that
obligately utilizes hydrocarbons. Int J Syst Evol Microbiol
52, 901–911.
Goodfellow, M. and Maldonado, L.A. (2006) The families
dietziaceae, gordoniaceae, nocardiaceae and
tsukamurellaceae. In The prokaryotes ed. Dworkin, M.,
Falkow, S., Rosenberg, E., Schleifer, K.H. and
Stackebrandt, E. pp. 843–888. New York, NY: Springer.
Hara, A., Syutsubo, K. and Harayama, S. (2003) Alcanivorax
which prevails in oil-contaminated seawater exhibits broad
substrate specificity for alkane degradation. Environ
Microbiol 5, 746–753.
Hara, A., Baik, S.H., Syutsubo, K., Misawa, N., Smits, T.H.,
van Beilen, J.B. and Harayama, S. (2004) Cloning and
functional analysis of alkB genes in Alcanivorax
borkumensis SK2. Environ Microbiol 6, 191–197.
Harayama, S., Kasai, Y. and Hara, A. (2004) Microbial
communities in oil-contaminated seawater. Curr Opin
Biotechnol 15, 205–214.
Hassanshahian, M., Emtiazi, G. and Cappello, S. (2012)
Isolation and characterization of crude-oil-degrading
bacteria from the Persian Gulf and the Caspian Sea.
Marine Poll Bull 64, 7–12.
Hedlund, B.P., Geiselbrecht, A.D., Bair, T.J. and Staley, J.T.
(1999) Polycyclic aromatic hydrocarbon degradation by a
new marine bacterium, Neptunomonas naphthovorans gen.
nov., sp. nov. Appl Environ Microbiol 65, 251–259.
Hendrickx, B., Junca, H., Vosahlova, J., Lindner, A., R€ uegg, I.,
Bucheli-Witschel, M., Faber, F., Egli, T. et al. (2006)
Alternative primer sets for PCR detection of genotypes
involved in bacterial aerobic BTEX degradation:
distribution of the genes in BTEX degrading isolates and
in subsurface soils of a BTEX contaminated industrial site.
J Microbiol Methods 64, 250–265.
Kasai, Y., Kishira, H., Sasaki, T., Syutsubo, K., Watanabe, K.
and Harayama, S. (2002) Predominant growth of
Alcanivorax strains in oil-contaminated and nutrientsupplemented sea water. Environ Microbiol 4, 141–147.
Kloos, K., Munch, J.C. and Schloter, M. (2006) A new method
for the detection of alkane-monooxygenase homologous
genes (alkB) in soils based on PCR-hybridization. J
Microbiol Methods 66, 486–496.
Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic acid
techniques in bacterial systematics ed. Stackebrandt, E. and
Goodfellow, M. pp. 115–175. New York: Wiley.
Lo Piccolo, L., De Pasquale, C., Fodale, R., Puglia, A.M. and
Quatrini, P. (2011) Involvement of an alkane hydroxylase
system of Gordonia sp. strain SoCg in degradation of
solid n-alkanes. Appl Environ Microbiol 77, 1204–1213.
Mahjoubi, M., Jaouani, A., Guesmi, A., Amor, S.B., Jouini, A.,
Cherif, H., Najjari, A., Boudabous, A. et al. (2013)
Hydrocarbonoclastic bacteria isolated from petroleum
contaminated sites in Tunisia: isolation, identification and
characterization of the biotechnological potential. N
Biotechnol 30, 723–733.
Malik, Z. and Ahmed, S. (2012) Degradation of petroleum
hydrocarbons by oil field isolated bacterial consortium.
Afr J Biotechnol 11, 650–658.
McKew, B.A., Coulon, F., Yakimov, M.M., Denaro, R.,
Genovese, M., Smith, C.J., Osborn, A.M., Timmis, K.N.
et al. (2007) Efficacy of intervention strategies for
bioremediation of crude oil in marine systems and effects
on indigenous hydrocarbonoclastic bacteria. Environ
Microbiol 9, 1562–1571.
M’rassi, A.G., Bensalah, F., Gury, J. and Duran, R. (2015)
Isolation and characterization of different bacterial strains
for bioremediation of n-alkanes and polycyclic aromatic
hydrocarbons. Environ Sci Poll Res 22, 15332–15346.
Muyzer, G., De Waal, E.C. and Uitterlinden, A.G. (1993)
Profiling of complex microbial populations by denaturing
gradient gel electrophoresis analysis of polymerase chain
reaction-amplified genes coding for 16S rRNA. Appl
Environ Microbiol 59, 695–700.
Porter, K.G. and Feig, Y.S. (1980) The use of DAPI for
identifying and counting aquatic microflora 1. Limnol
Oceanogr 25, 943–948.
Quatrini, P., Scaglione, G., De Pasquale, C., Riela, S. and
Puglia, A.M. (2008) Isolation of Gram-positive nalkane degraders from a hydrocarbon-contaminated
Mediterranean shoreline. J Appl Microbiol 104, 251–
259.
Rajaei, S., Seyedi, S.M., Raiesi, F., Shiran, B. and Raheb, J.
(2013) Characterization and potentials of indigenous oildegrading bacteria inhabiting the rhizosphere of wild oat
(Avena fatua L.) in South West of Iran. Iran J
Biotechnol 11, 32–40.
R€ oling, W.F., Milner, M.G., Jones, D.M., Lee, K., Daniel, F.,
Swannell, R.J. and Head, I.M. (2002) Robust hydrocarbon
degradation and dynamics of bacterial communities
during nutrient-enhanced oil spill bioremediation. Appl
Environ Microbiol 68, 5537–5548.
Santisi, S., Cappello, S., Catalfamo, M., Mancini, G.,
Hassanshahian, M., Genovese, L., Giuliano, L. and
Journal of Applied Microbiology 126, 780--795 © 2018 The Society for Applied Microbiology
794
The use of oil-degrading bacteria as an alternative for environmental remediation (bioremediation)
N. Djahnit et al.