Restricted accessResearch articleFirst published online 2015-10
Effects of Heavy Metals on Biodegradation of Fluorene by a Sphingobacterium sp. Strain (KM-02) Isolated from Polycyclic Aromatic Hydrocarbon-Contaminated Mine Soil
The present study investigated fluorene biodegradation by Sphingobacterium sp. KM-02 in the presence of heavy metals. A fluorene-degrading strain of Sphingobacterium was isolated from polycyclic aromatic hydrocarbon-contaminated soil near a mine-impacted area in Korea. When Sphingobacterium sp. KM-02 was grown in a medium with fluorene as the sole carbon source, it removed 78.4% of this compound within 120 h. Identification of the metabolic intermediates (9-fluorenone, 4-hydroxy-9-fluorenone, and 8-hydroxy-3,4-benzocoumarin) were also performed. Composting experiments under laboratory conditions indicated that this microbe also removed fluorene from contaminated soil. In particular, treatment of microcosm soil with strain KM-02 for 20 days resulted in a 65.6% reduction of fluorene concentration. Experiments of effects of heavy metals on fluorene removal by strain KM-02 showed that 10 mg/L cadmium, copper, zinc, and lead, reduced growth and fluorene degradation by this microbe. Cadmium and copper had strong effects at 10 mg/L, although zinc and lead had relatively slight inhibitory effect at concentrations of 10 and 100 mg/L. Arsenic had no effect on the growth or fluorene degradation, even at 100 mg/L.
Get full access to this article
View all access options for this article.
References
1.
AchtenC., and HofmannT. (2009). Native polycyclic aromatic hydrocarbons (PAH) in coals—A hardly recognized source of environmental contamination. Sci. Total. Environ., 407, 2461.
2.
AmorL., KennesC., and VeigaM.C. (2001). Kinetics of inhibition in the biodegradation of monoaromatic hydrocarbons in presence of heavy metals. Bioresour. Technol., 78, 181.
3.
Antizar-LadislaoB., Lopez-RealJ.M., and BeckA.J. (2006). Bioremediation of polycyclic aromatic hydrocarbons (PAH) in an aged coal-tar-contaminated soil using different in-vessel composting approaches. J. Hazard. Mater., 137, 1583.
4.
BaathE. (1989). Effect of heavy metals in soil on microbial processes and population. Water Air Soil Pollut., 47, 335.
5.
Banach-SzottM., DebskaB., and RosaE. (2014). Effect of soil pollution with polycyclic aromatic hydrocarbons on the properties of humic acids. J. Soils Sediments, 14, 1169.
6.
BoldrinB., TiehmA., and FritzscheC. (1993). Degradation of phenanthrene, fluorene, fluoranthene, and pyrene by a Mycobacterium sp. Appl. Environ. Microbiol., 59, 1927.
7.
BruinsM.R., KapilS., and OehmeF.W. (2000). Microbial resistance to metals in the environment. Ecotoxicol. Environ. Saf., 45, 198.
8.
CasellasM., GrifollM., BayonaJ.M., and SolanasA.M. (1997). New metabolites in the degradation of fluorene by Arthrobacter sp. strain F101.Appl. Environ. Microbiol., 63, 819.
9.
ChenS., YinH., YeJ., PengH., ZhangN., and HeB. (2013). Effect of copper(II) on biodegradation of benzo[a]pyrene by Stenotrophomonas maltophilia. Chemosphere, 90, 1811.
10.
El AdnaniM., Rodriguez-MarotoJ.M., SbaiM.L., LoukiliI.L., and NejmeddineA. (2007). Impact of polymetallic mine (Zn, Pb, Cu) residues on surface water, sediments and soils at the vicinity (Marrakech, Morocco). Environ. Technol., 28, 969.
11.
GanS., LauE.V., and NgH.K. (2009). Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). J. Hazard. Mater., 172, 532.
12.
GrifollM., SelifonovS.A., and ChapmanP.J. (1994). Evidence for a novel pathway in the degradation of fluorene by Pseudomonas sp. strain F274. Appl. Environ. Microbiol., 60, 2438.
13.
GrifollM., SelifonovS.A., and ChapmanP.J. (1995). Transformation of substituted fluorenes and fluorene analogs by Pseudomonas sp. strain F274. Appl. Environ. Microbiol., 61, 3490.
14.
HabeH., ChungJ.S., KatoH., AyabeY., KasugaK., YoshidaT., NojiriH., YamaneH., and OmoriT. (2004). Characterization of the upper pathway genes for fluorene metabolism in Terrabacter sp. strain DBF63. J. Bacteriol., 186, 5938.
15.
HattoriH. (1992). Influence of heavy metals on soil microbial activities. Soil Sci. Plant Nutr., 38, 93.
16.
HelbigK., GrosseC., and NiesD.H. (2008). Cadmium toxicity in glutathione mutants of Escherichia coli. J. Bacteriol., 190, 5439.
17.
HeuerH., KrsekM., BakerP., SmallaK., and WellingtonE.M. (1997). Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol., 63, 3233.
18.
HongH.B., NamI.H., KimY.M., ChangY.S., and SchmidtS. (2007). Effect of heavy metals on the biodegradation of dibenzofuran in liquid medium. J. Hazard. Mater., 140, 145.
19.
JiG., and SilverS. (1992). Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J. Bacteriol., 174, 3684.
20.
KanalyR.A., and HarayamaS. (2000). Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J. Bacteriol., 182, 2059.
21.
KeithL.H., and TelliardW.A. (1979). Priority pollutants. I. A perspective view. Environ. Sci. Technol., 13, 416.
22.
LinC.W., ChenS.Y., and ChengY.W. (2006). Effect of metals on biodegradation kinetics for methyl tert-butyl ether. Biochem. Eng. J., 32, 25.
23.
LuL., and ZhuL. (2012). Effect of soil components on the surfactant-enhanced soil sorption of PAHs. J. Soils Sediments, 12, 161.
24.
MittalS.K., and RatraR.K. (2000). Toxic effect of metal ions on biochemical oxygen demand. Water Res., 34, 147.
25.
MonnaL., OmoriT., and KodamaT. (1993). Microbial degradation of dibenzofuran, fluorene, and dibenzo-p-dioxin by Staphylococcus auriculans Dbf63. Appl. Environ. Microbiol., 59, 285.
26.
Moreno-JimenezE., PeñalosaJ.M., ManzanoR., Carpena-RuizR.O., GamarraR., and EstebanE. (2009). Heavy metals distribution in soils surrounding an abandoned mine in NW Madrid (Spain) and their transference to wild flora. J. Hazard. Mater., 162, 854.
27.
MostertM.M., AyokoG.A., and KokotS. (2010). Application of chemometrics to analysis of soil pollutants. Trends Anal. Chem., 29, 430.
28.
NamI.H., HongH.B., KimY.M., KimB.H., MurugesanK., and ChangY.S. (2005). Biological removal of polychlorinated dibenzo-p-dioxins from incinerator fly ash by Sphingomonas wittichii RW1. Water Res., 39, 4651.
29.
NamI.H., KimY.M., MurugesanK., JeonJ.R., ChangY.Y., and ChangY.S. (2008). Bioremediation of PCDD/Fs-contaminated municipal solid waste incinerator fly ash by a potent microbial biocatalyst. J. Hazard. Mater., 157, 114.
30.
NamI.H., KimY.M., SchmidtS., and ChangY.S. (2006). Biotransformation of 1,2,3-tri- and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin by Sphingomonas wittichii strain RW1. Appl. Environ. Microbiol., 72, 112.
PagnoutC., FracheG., PoupinP., MaunitB., MullerJ.F., and FérardJ.F. (2007). Isolation and characterization of a gene cluster involved in PAH degradation in Mycobacterium sp. Strain SNP11: Expression in Mycobacterium smegmatis mc2 155. Res. Microbiol., 158, 175.
33.
PepiM., VolterraniM., RenziM., MarvasiM., GasperiniS., FranchiE., and FocardiS.E. (2007). Arsenic-resistant bacteria isolated from contaminated sediments of the Orbetello Lagoon, Italy, and their characterization. J. Appl. Microbiol., 103, 2299.
34.
RiisV., BabelW., and PucciO.H. (2002). Influence of heavy metals on the microbial degradation of diesel fuel. Chemosphere, 49, 559.
35.
SaidW.A., and LewisD.L. (1991). Quantitative assessment of the effects of metals on microbial degradation of organic chemicals. Appl. Environ. Microbiol., 57, 1498.
36.
SchulerL., Ni ChadhainS.M., JouanneauY., MeyerC., ZylstraG.L., HolsP., and AgathosS.N. (2008). Characterization of a novel angular dioxygenase from fluorene-degrading Sphingomonas sp. strain LB126. Appl. Environ. Microbiol., 74, 1050.
37.
SokhnJ., De LeijF.A., HartT.D., and LynchJ.M. (2001). Effect of copper on the degradation of phenanthrene by soil microorganisms. Lett. Appl. Microbiol., 33, 164.
38.
StorelliM.M., and MarcotrigiganoG.O. (2000). Polycyclic aromatic hydrocarbon distributions in sediment from the Mar Piccolo, Ionian Sea, Italy. Bull. Environ. Contam. Toxicol., 65, 537.
39.
SultanS., and HasnainS. (2003). Pseudomonad strains exhibiting high level Cr(VI) resistance and Cr(VI) detoxification potential. Bull. Environ. Contam. Toxicol., 71, 473.
40.
ThangarajK., KapleyA., and PurohitH.J. (2008). Characterization of diverse Acinetobacter isolates for utilization of multiple aromatic compounds. Bioresour. Technol., 99, 2488.
41.
ThorntonI. (1996). Impacts of mining on the environment: Some local, regional and global issues. Appl. Geochem., 11, 355.
42.
TrenzS.P., EngesserK.H., FischerP., and KnackmussH.J. (1994). Degradation of fluorene by Brevibacterium sp. strain DPO 1361: A novel C-C bond cleavage mechanism via 1,10-dihydro-1,10-dihydroxyfluoren-9-one. J. Bacteriol., 176, 789.
43.
TylerG. (1974). Heavy metal pollution and soil enzymatic activity. Plant Soil, 41, 303.
44.
WangR., LiuG., ChouC.L., LiuJ., and ZhangJ. (2010). Environmental assessment of PAHs in soils around the Anhui coal district, China. Arch. Environ. Contam. Toxicol., 59, 62.
45.
WattiauP., BastiaensL., van HerwijnenR., DaalL., ParsonsJ.R., RenardM.-E., SpringaelD., and CornelisG.R. (2001). Fluorene degradation by Sphingomonas sp. LB126 proceeds through protocatechuic acid: A genetic analysis. Res. Microbiol., 152, 861.
46.
WilckeW. (2007). Global patterns of polycyclic aromatic hydrocarbons (PAHs) in soil. Geoderma, 141, 157.
