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A novel Pseudomonas strain was iso- Long chain alkanes and polycyclic aromatic hydrocarbons have been threatening the global environment
lated from heavy oil contaminated because of toxicity and poor bioavailability. We isolated one novel Pseudomonas strain from heavy-oil con-
soil. taminated soil which could degrade long-chain alkanes and polycyclic aromatic hydrocarbons (PAHs) and
It can convert n-alkanes and poly- could produce the surfactin, fengycin and lichenysin, which are mostly recognized as common metabo-
cyclic aromatic hydrocarbons to lites produced by Bacillus sp. And the heavy oil could be easily and efciently removed from quartz sand
lipopeptides surfactant. by these lipopeptides. This paper showed that Pseudomonas is the excellent degrader of alkanes and PAHs
Lipopeptides surfactant have differ- and produce the well-known rhamnolipids and the easily neglected lipopeptides.
ent structures when using different
hydrocarbons.
Lipopetides surfactant showed great
performance on heavy oil sand wash-
ing.
a r t i c l e i n f o a b s t r a c t
Article history: Alkanes and polycyclic aromatic hydrocarbons (PAHs) have threatened the environment due to toxicity
Received 17 March 2014 and poor bioavailability. Interest in degradation of these hazardous materials by biosurfactant-producing
Received in revised form 25 April 2014 bacteria has been steadily increasing in recent years. In this work, a novel biosurfactant-producing Pseu-
Accepted 22 May 2014
domonas sp. WJ6 was isolated to degrade a wide range of n-alkanes and polycyclic aromatic hydrocarbons.
Available online 2 June 2014
Production of lipopeptide biosurfactant was observed in all biodegradable studies. These lipopeptides
were puried and identied by C18 RP-HPLC system and electrospray ionization-mass spectrometry.
Keywords:
Results of structural analysis showed that these lipopeptides generated from different hydrocarbons
n-Alkane
Aromatic hydrocarbons
were classied to be surfactin, fengycin and lichenysin. Heavy-oil sludge washing experiments demon-
Biodegradation strated that lipopeptides produced by Pseudomonas sp. WJ6 have 92.46% of heavy-oil washing efciency.
Lipopeptides The obtained results indicate that this novel bacterial strain and its lipopeptides have great potentials in
Pseudomonas the environmental remediation and petroleum recovery.
2014 Elsevier B.V. All rights reserved.
Corresponding authors at: Power Environmental Energy Research Institute, 738 Arrow Grand Circle, Covina, CA 91722, USA. Tel.: +1 626 250 4448/+86 10 62529069/
+1 626 858 5077; fax: +1 626 858 5077/+86 10 62529069/+1 626 858 5077.
E-mail addresses: wenjie.hsia@gmail.com, sjkr5201314@gmail.com (W. Xia), fuyi.wang@iccas.ac.cn (F. Wang), yongchun.tang@peeri.org (Y. Tang).
http://dx.doi.org/10.1016/j.jhazmat.2014.05.062
0304-3894/ 2014 Elsevier B.V. All rights reserved.
490 W. Xia et al. / Journal of Hazardous Materials 276 (2014) 489498
anaerobic, oval to rod-shaped (0.30.5 m 0.51.0 m), and C40) and PAHs (uorene, naphthalene, phenanthrene, pyrene)
motile with single agellum. Colonies (0.52 mm) growing on were tested as the sole carbon sources, the growth of strain WJ6
LB agar for 2 days at 37 C were smooth, circular convex, wet was observed in all cases. It grew obviously and rapidly with n-
and yellowish-brown in color. The organism was able to grow at alkanes (C12, C22, and C32), while it grew a bit slower when
550 C, pH 410 and 015% (w/v) NaCl, with the optimum growth utilizing C40 and polycyclic aromatic hydrocarbons, as shown in
occurring at pH 6.57.5, 37 C and 02% (w/v) NaCl. It was positive Fig. 2. Comparisons with Pseudomonas strains reported by some
for catalase, urease, oxidase, aerobic nitrite reduction, anaerobic literatures indicated that strain WJ6 could use a broader range of
nitrate reduction and denitrication, as well as for the hydrolysis of crude oil components as the sole carbon sources, including aliphatic
starch and gelatin. Morphological, physiological and phylogenetic hydrocarbons, branched alkane, cyclane and aromatic hydrocar-
properties indicated that strain WJ6 was a member of the genus bons [14,25].
Pseudomonas, and the Genbank accession number is KF155141. When utilizing the n-alkanes, a remarkable increase of CFU
counts was observed from 8 days to 12 days (Fig. 2ad). The
3.2. Biodegradation of n-alkanes and PAHs maximum CFU counts decreased with the chain-length increas-
ing. Stationary phase started on the 12th days for n-alkanes C12
Longer chain n-alkanes and PAHs in crude oil were generally and C22, while delayed by nearly 4 days for C32 and C40. Specif-
considered to be only slightly biodegradable due to their higher ically, n-dodecane (C12) was degraded by 46.65% in the 20-days
hydrophobicity [8,33]. In this work, n-alkanes (C12, C22, C32 and degradation. Comparatively, only 42.62%, 31.69% and 23.62% of C22,
Fig. 2. Degradation of different n-alkanes and polycyclic aromatic hydrocarbons as the sole carbon sources by Pseudomonas sp. WJ6. Opened square ( ) stands for residual
hydrocarbon in right vertical axis; Filled triangle ( ) stands for CFU count in the left vertical axis. (A)(D) represent the case of n-alkane C12, C22, C32 and C40; (E)(H)
represent the case of PAHs uorene, naphthalene, phenanthrene and pyrene, respectively. The values are mean standard deviations (n = 3).
W. Xia et al. / Journal of Hazardous Materials 276 (2014) 489498 493
C32 and C40 were degraded, respectively (Fig. 2bd). The mecha- dibenzothiophene. Herein, this newly Pseudomonas sp. WJ6 can
nism of alkane biodegradation has been widely studied, and the degrade both alkanes and PAHs efciently. However, the metabolic
metabolic pathway, alkanehydroxylases enzymes and gene clus- mechanism of the degradation of long-chain alkane and PAHs about
ters have been examined in details [34,35]. However, most studies strain WJ6 remains uncertain. Further works about the degradation
on the degradation pathways of alkanes have focused on short- mechanism will focus on the hydrophilic or hydrophobic charac-
or medium-chain alkanes. Microorganisms degrading short-chain teristic of cell surface, hydroxylase enzymes and gene cluster of
alkanes (C2C4) have enzymes related to methane monooxyge- alkane or PAHs degradation.
nase [36], while strains degrading medium-chain alkanes (C5C11)
or long-chain alkane (>C12) frequently contain integral membrane 3.3. TLC analysis of puried biosurfactant
non-heme iron monooxygenase related to the well-characterized
Pseudomonas putida GPo1 Alkb alkane hydroxylase [37]. Some In terms of the results of hydrocarbon degradation and cell
strains contain alkane hydroxylating enzymes that belong to a fam- growth, the biosurfactants partially puried from the cultures of
ily of soluble cytochrome P-450s and that against C5C11 alkanes biodegradation of hydrocarbons (n-dodecane, uorene and pyrene)
[38]. In additions, several bacterial strains have been reported to were selected and analyzed by thin layer chromatography (Fig. 3).
assimilate alkanes larger than C20 [25,39]. However the enzymes Three biosurfactants have an identical Rf value of 0.74 and showed
responsible for the oxidation of long-chain alkanes are still poorly positive reactions with two spray reagents of ninhydrin and iodine,
characterized and only recently have started to be character- indicating three biosurfctants maybe belongs to lipopeptide and
ized. consisted of peptide and lipid moieties.
PAHs are pollutants to environments because of their toxic and
carcinogenic potentials. Due to the high hydrophobicity of aromatic 3.4. Structural analysis of biosurfactant
rings, PAHs are much more resistant to biodegradation. However
degradation of PAHs by Pseudomonas sp. WJ6 was remarkable. As The partially puried biosurfactant produced by the WJ6 strain
shown in Fig. 2eh, uorene, naphthalene and phenanthrene were with using hydrocarbons (n-dodecane, uorene, pyrene) were
obviously degraded, respectively, by 39.45%, 23.14% and 21.93% in subjected to the reverse-phase HPLC. With a linear gradient of ace-
20 d. Compared to PAHs of two and three aromatic rings, pyrene tonitrile and water, three biosurfactants were resolved into several
that contain four aromatic rings were much more resistant to fractions as shown in Fig. 4.
biodegradation with 19.50% of pyrene degraded. Degradation of The separated HPLC fractions were then tested for surface activ-
PAHs by microorganisms was extensively studied throughout the ity by the drop-collapsing assay, the fractions that reduce the
world [40]. Pseudomonas strains have been reported to degrade n- surface tension were collected and the amino acid moieties were
alkanes and PAHs [35]. Pseudomonas sp. F274 [41], Pseudomonas analyzed and listed in Table 1.
sp. NCIB 9816-4 [42] and P. putida F1 [43] were isolated and HPLC fractions were also analyzed by electrospray ionization
found to have the ability to degrade uorene, dibenzofuran and mass spectrometry (ESI-MS) coupled to the HPLC system. As shown
in Fig. 5a, a series of singly-charged negative ions were observed for
the fraction 1 of the n-dodecane sample eluting at 10.46 min, hav-
ing a 14 Da difference in mass between the neighboring ion peaks.
Fig. 5. Mass spectra of the HPLC fractions eluting at (a) 10.46, (b) 13.03, (c) 28.95, (d) 30.98 and (e) 33.23 min as shown in Fig. 4A of the biosurfactants produced by Pseudomonas
sp. WJ6 using n-dodecane as carbon source.
Based on the fatty acid (data not shown) and amino acid analysis, The MS under negative mode showed deprotonated molecular
the ve ions are assignable to the deprotonated homologs [M H] ions [M H] at m/z 1075, 1047, 1031, 1019 and 1005 with m/z
([M H] at m/z 1447, 1461, 1475, 1491 and 1503) of the fengyin 1031, 1047 and 1075 being the main ions for the HPLC fraction 2
A lipopeptides (Table 2) which compose of ten amino acids linked eluting at 13.03 of n-dodecane sample (Fig. 5b). Yakimov et al. [48]
to a C15, C16, C17, C18 or C19 hydroxy fatty acid chain, respec- reported that the ve ion peaks have a 14 Da or 28 Da difference
tively. Moreover, four minor ions peaks were observed at m/z 1469, in mass each another, except the ion at m/z 1031, possibly has one
1497, 1513 and 1525 which correspond to the sodiated molecules double bond referring to the deprotonated molecular ions. Coupling
[M + Na] (Fig. 5a). These spectra are very similar to those reported with the fatty acid (data not shown) and amino acid analysis, such
in the literature [4447], where protonated ions [M + H]+ at m/z a distribution of molecular ions is in excellent agreement with that
1435.6, 1449.9, 1463.7, 1477.8, 1491.7 and 1505.9 were observed of the lichenysin A lipopeptides homologs (Table 2), and the main
for fengycin homologs under positive MS mode. -hydroxy fatty acid residues in the lipophilic moiety of lichenysin
Table 1
The amino acid moieties of surface active fractions arising from RP-HPLC separation of biosurfactants produced by the WJ6 strain with using various hydrocarbons as carbon
source. The HPLC chromatograms are shown in Fig. 4.
Hydrocarbon Surface active fraction HPLC retention time (min) Amino acid moiety
n- Fraction 1 10.46 2 Glu, 1 Gln, 1 Orn, 2 Tyr, 1 Thr, 1 Ala, 1 Pro, 1Ile
Dodecane Fraction 2 13.03 1 Gln, 3Leu, 2 Val, 1 Asp, 1 IIe
Fraction 3 28.95 1 Glu, 3 Leu, 2 Val, 1 Asp
Fraction 4 30.98 1 Glu, 4 Leu, 1 Val, 1 Asp
Fraction 5 33.23 1 Glu, 3 Leu, 1 Val, 1 Asp, 1 IIe
Fluorene Fraction 6 7.49 2 Glu, 1 Gln, 1 Orn, 2 Tyr, 1 Thr, 1 Ala, 1 Pro, 1 Val
Fraction 7 10.13 1 Gln, 3Leu, 1 Val, 1 Asp, 1 IIe
Pyrene Fraction 8 8.44 2 Glu, 1 Gln, 1 Orn, 2 Tyr, 1 Thr, 1 Ala, 1 Pro, 1 Val
Fraction 9 13.91 1 Gln, 3Leu, 1 Val, 1 Asp, 1 IIe
W. Xia et al. / Journal of Hazardous Materials 276 (2014) 489498 495
Table 2
Lipopeptides produced by Pseudomonas sp. WJ6 with three hydrocarbons as carbons source.
Fengycin Fraction 1: Fengycin A [Ala6]-(C15, Fraction 6: Fengycin A [Ala6]-C14, Fraction 8: Fengycin A [Ala6]-C15.
C16, C17, C18, C19) [Ala6]-C15, [Ala6]-C19.
Lichenysin Fraction 2: Lichenysin A (C13,C14, C15, Fraction 7: Lichenysin A (C14, C15, C16, Fraction 9: Lichenysin A (C15, C16, C17
C16, C17), C15 has one double bond C18), C15 has one double bond C18), C15 has one double bond
A molecules are assignable to C13, C14, C15 (containing one double are assigned to be C14, C15 (containing a double bonds), C16 and
bond), C16 and C17, respectively. C18, respectively, similar to the results reported in the literature
For the n-dodecane sample, the negative MS mode analysis [49].
observed three deprotonated molecular ions [M H] at m/z 994, Two fractions, which showed surface active (Fig. 4c, Table 1)
1008 and 1022 for the fraction 3 eluting at 28.95 min (Fig. 5c), two arising from the HPLC separation of the pyrene sample were ana-
deprotonated molecular ions at m/z 1008 and 1022 for the fraction 4 logically analyzed by MS under negative mode. The results showed
eluting at 30.98 min (Fig. 5d), and two deprotonated molecular ions deprotonated molecular ions [M H] at m/z 1447 for the rst
at m/z 1022 and 1036 for the fraction 5 eluting at 33.23 min (Fig. 5e). fraction 8 eluting at 8.44 min (Fig. 7a). Combined with amino acid
These ion peaks have a 14 Da difference in mass each another, indi- analyses, the mass of this species is in excellent agreement with that
cating that these biosurfactants maybe belong to the homologs of of the fengycin A lipopeptides which composed of ten amino acids
lipopeptides. Pereira et al. [49] has described the surfactin mix- linked to a C15 -hydroxy fatty acid chain (Table 2) with similar
ture extract has protonated peaks with sodium adducts [M + Na]+ reported in the literature [40]. For the second fraction (fraction 9)
at m/z 1030.6, 1044.6 and 1058.7. Kowall et al. [28] described twelve eluting at 13.91 min, the negative MS showed deprotonated molec-
surfactins with molecule weight of 994, 1008, 1022 and 1036 Da, ular ions [M H] at m/z 1031, 1047, 1061 and 1075 (Fig. 7b). Taking
which contain different amino acids when same molecule weight the amino acid analysis result into account (Table 1), such a distri-
achieved. Therefore, in terms of the fatty acid (data not shown) bution of molecular ions is in excellent agreement with that the
and amino acid analysis, such a distribution of molecular ions of
fractions (fraction 3 to 5) is in excellent agreement with that of
the surfactin lipopeptides (Table 2). Fraction 3 was surfactin with
L-Val in position 7 of peptide ring linked with -hydroxy fatty
acid with chain lengths of 1315 carbon atoms; the fraction 4 con-
tains surfactins with L-Leu in position 7 of peptide ring linked with
-hydroxy fatty acid with chain lengths of 1314 carbon atoms.
Fraction 5 was surfactin with L-Ile in position 7 of peptide ring
linked with -hydroxy fatty acid with chain lengths of 1415 car-
bon atoms.
About the uorene sample, two fractions appeared to be drop-
collapsing active were collected and the corresponding analysis of
the amino acid showed in Table 1. The MS under negative mode
of MS showed deprotonated molecular ions [M H] at m/z 1433,
1447 and 1503 for the fraction 6 eluting at 7.49 min (Fig. 6a).
These results indicated that the distribution of molecular ions of
this fraction is in excellent agreement with that of the fengycin A
lipopeptides (Table 2), which composed of ten amino acids linked
to a C14, C15 or C19 -hydroxy fatty acid chain. The mass-spec
spectra reported are very similar to those obtained by Bie et al.
[45]. For the fraction 7 eluting at 10.13, four deprotonated molecu-
lar ions [M H] at m/z 1017, 1031, 1047 and 1075 were observed.
Combined with the amino acid analysis (Table 1), such a distribu-
tion of molecular ions is in excellent agreement with that of the
Fig. 6. Mass spectra of the HPLC fractions eluting at (a) 7.49 and (b) 10.13 min
lichenysin A lipopeptides (Table 2), and the main -hydroxy fatty
as shown in Fig. 4B of the biosurfactants produced by Pseudomonas sp. WJ6 using
acid residues in the lipophilic part of the lichenysin A homologs uorine as carbon source.
496 W. Xia et al. / Journal of Hazardous Materials 276 (2014) 489498
Fig. 7. Mass spectra of the HPLC fractions eluting at (a) 8.44 and (b) 13.91 min
as shown in Fig. 4C of the biosurfactants produced by Pseudomonas sp. WJ6 using
pyrene as carbon source.
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