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Previous Article | Next Article 
Appl Environ Microbiol, June 1998, p. 2327-2331, Vol. 64, No. 6
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Desulfurization of Dibenzothiophene and Diesel Oils
by a Newly Isolated Gordona Strain, CYKS1
Sung-Keun
Rhee,
Je Hwan
Chang,
Yong Keun
Chang,* and
Ho Nam
Chang
BioProcess Engineering Research Center and
Department of Chemical Engineering, Korea Advanced Institute of
Science and Technology, 373-1, Kusong-dong, Yusung-gu, Taejon
305-701, Korea
Received 9 January 1998/Accepted 30 March 1998
 |
ABSTRACT |
A dibenzothiophene (DBT)-desulfurizing bacterial strain was
isolated and identified as Gordona strain CYKS1. Strain
CYKS1 was found to transform DBT to 2-hydroxybiphenyl via the 4S
pathway and to be able to also use organic sulfur compounds other than DBT as a sole sulfur source. Its desulfurization activity was susceptible to sulfate repression. Active resting cells for
desulfurization could be prepared only in the early growth phase. When
two types of diesel oils, middle distillate unit feed (MDUF) and light
gas oil (LGO) containing various organic sulfur compounds including DBT, were treated with resting cells of strain CYKS1 for 12 h, the
total sulfur content significantly decreased, from 0.15% (wt/wt) to
0.06% (wt/wt) for MDUF and from 0.3% (wt/wt) to 0.25% (wt/wt) for
LGO. The newly isolated strain CYKS1 is considered to have good
potential for application in the biodesulfurization of fossil fuels.
| |
TEXT |
All fossil fuels contain organic
sulfur compounds. When fossil fuels are combusted, sulfur dioxide
generated from organic sulfur compounds is released into the
atmosphere, causing air pollution. To remove sulfur from fossil fuels,
refiners now rely on a hydrodesulfurization technique, which is costly
and energy-intensive and not effective at removing polycyclic sulfur
compounds (4). Therefore, microbial desulfurization has
attracted attention for its application to the desulfurization of coal
and petroleum.
A variety of sulfur-containing heterocyclic organic compounds in fossil
fuels have been characterized. Since dibenzothiophene (DBT) is a
typical recalcitrant organic sulfur compound in fossil fuels,
desulfurization of DBT has been a model reaction in the treatment of
fossil fuels. There have been several reports on the isolation of
DBT-desulfurizing bacteria. Species of Brevibacterium and
Pseudomonas utilize DBT as the sole source of carbon,
sulfur, and energy (14, 23). Under anaerobic conditions,
biphenyl was formed from DBT by Desulfovibrio desulfuricans
M6 (26). Microbial systems have also been reported to
selectively abstract the sulfur heteroatom from this model heterocycle.
Rhodococcus rhodochrous IGTS8, Rhodococcus
erythropolis D-1, and Corynebacterium sp. strain SY1
were observed to remove only sulfur from DBT, converting DBT to
2-hydroxybiphenyl (2-HBP) (6, 8, 17). The selective removal
of organic sulfur by these strains looks promising for the treatment of
fuel oils using an aqueous cell suspension, since valuable combustible
compounds are retained in this reaction without being broken down into
water-soluble compounds. However, there are only a few reports on the
treatment of diesel oils with these isolated strains.
In this article, we describe the characteristics of DBT desulfurization
by a newly isolated bacterial strain, CYKS1, and demonstrate the
possibility of its application for the biocatalytic desulfurization of
diesel oils.
Enrichment and isolation of DBT-desulfurizing microorganisms.
Deionized water (resistance = 20 M
· cm) was used to
prepare all sulfur-free minimal salt medium (MSM) and stock solutions. The MSM contained, per liter of deionized water, 5.0 g of glucose, 5.0 g of K2HPO4, 1.0 g of
NaH2PO4, 1.0 g of NH4Cl,
0.2 g of MgCl2, 0.01 g of CaCl2
· 2H2O, 1 ml of sulfur-free trace element solution dissolved with EDTA (21), and 1 ml of vitamin solution
(25). DBT was dissolved in ethanol to a concentration of 100 mM and added to a sterilized basal MSM. Enrichment cultures were
initiated by inoculating MSM containing 1 mM DBT with 10% (vol/vol)
oil-contaminated wastewater discharged from the dye industry complex in
Taegu, Korea. The cultures were performed in 250-ml Erlenmeyer flasks with 50 ml of MSM at 30°C on a gyratory shaker. All the data shown in
this work are the mean values of data from duplicate or triplicate experiments. Determination of DBT and its metabolites was carried out
by the method described previously (8). The culture broth or
reaction mixture was acidified to pH 2.0 with 1 N HCl and extracted with 1 volume of ethyl acetate. A portion of the ethyl acetate layer
was removed, and 10 µl of the supernatant was injected into a
reverse-phase high-performance liquid chromatograph (Hitachi model
L-6200, L-4200H UV-VIS detector) equipped with a µBondapak phenyl
column (3.9 by 300 mm) (Waters, Milford, Mass.) and detected at 280 nm.
The mobile phase was 65% (vol/vol) methanol in water. In all
experiments involving extraction with ethyl acetate, carbazole was used
as the internal standard. The range of concentrations effective for the
quantification of DBT-related compounds was 0.02 to 12 mM.
Evidence of sulfur-specific desulfurization was obtained by the
high-performance liquid chromatography analysis of samples taken from
the broth of stationary-phase enrichment cultures. Only trace
concentrations (about 0.05 mM) of dibenzothiophene sulfone
(DBTO2) and 2-HBP were detected as transformation
products of DBT in primary enrichment culture. Sulfur-containing
contaminants in the bacterial sources might prevent the enrichment of
DBT-desulfurizing bacteria. After several transfers of enrichment
cultures, the concentration of 2-HBP produced increased to about 0.3 mM
in the stationary phase of cultures. It seemed that 2-HBP was the
dead-end product of DBT desulfurization, since the concentration of
2-HBP did not significantly decrease in the stationary phase.
Transfer cultures were plated on minimal solid medium spread with DBT.
For preparation of the medium, 200 µl of DBT stock solution (100 mM)
was spread onto a solid medium containing a sulfur-free MSM with agar.
After 2 weeks of incubation, individual colonies showing clear zones
were selected and tested in a DBT-containing MSM for the ability to
transform DBT to 2-HBP. Although clear zones might be indirect evidence
of DBT desulfurization, we could easily screen DBT-desulfurizing
bacteria by this method.
Identification of the isolated strain, CYKS1.
Isolated strains
were identified on the basis of their morphological, physiological, and
chemotaxonomical properties. A mucoid isolate, CYKS1, from the colonies
was an aerobic, nonmotile, nonspore-forming, and gram-positive
bacterium. CYKS1 bacteria were rod shaped, as observed by a light
microscope. However, when CYKS1 cells were stained, four to five
coccoid cells surrounded by a slimy material were found. The isolate
was catalase positive and oxidase positive. Preparation of
peptidoglycan and analysis of diaminopimelic acid isomer, isoprenoid
menaquinone, and cell wall sugar were carried out by previously
described methods (10). Strain CYKS1 had mycolic acid and
the meso form of diaminopimelic acid in the cell wall. The
major cell wall sugars were arabinose and galactose. This strain had
MK-9(H2) as the sole menaquinone. By comparing these results with the reported chemotaxonomic characteristics of coryneform bacteria (1, 22), we identified this strain as
Gordona strain CYKS1.
Characterization of DBT desulfurization by strain CYKS1.
Figure 1 shows the time course of DBT
utilization by strain CYKS1 in an MSM supplemented with 0.3 mM DBT as a
sole sulfur source. Cell growth was monitored by measuring the
absorbance of culture broth samples at 600 nm
(A600). Dry cell weight (DCW) was determined by
the method described previously (12). DBT and its
metabolites were determined by use of a gas chromatograph (GC) equipped
with a flame ionization detector (model 5890; Hewlett-Packard, Wilmington, Del.) and by mass spectrometry (MS; Fisons, Altrincham, England) as described by Denome et al. (3). An ethyl
acetate-extracted sample was dried over anhydrous sodium sulfate and
concentrated in a rotary evaporator, and the sample was then analyzed
by GC-MS. The GC analysis was conducted with an HP5 column (30 m by
0.32 mm [inside diameter]; 1.0-µm phase thickness). Because sulfone was thermally unstable, the injector temperature maintained was rather
low, at 250°C.
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FIG. 1.
Biodesulfurization of DBT by strain CYKS1 in a batch
culture. Symbols:  , cell growth;  , glucose concentration;  ,
DBT concentration;  , 2-HBP concentration.
|
|
The strain showed maximum growth (2.7 g [DCW]/liter) at 100 h of
cultivation. The pH decreased from 7.4 to 5.9. Desulfurization activity
and cell growth decreased about 23% according to this change in pH.
The major product accumulated was identified as 2-HBP by GC-MS.
Approximately 95% of the DBT was converted to 2-HBP, and the 2-HBP
concentration did not decrease during stationary phase. 2-HBP could
accumulate up to a concentration of 0.25 mM in the culture medium and
was not used as a carbon source for cell growth. When the effect of
2-HBP on the growth of strain CYKS1 was studied, the generation time of
strain CYKS1 was found to increase by about 50% in the presence of 0.2 mM 2-HBP. The strain could grow even at 0.30 mM 2-HBP but only with a
very long generation time. Considering the report that the inhibitory
effect of 2-HBP was the main limiting factor of the desulfurization of DBT (17), the resistance of strain CYKS1 to inhibition by
2-HBP was similar to that of any other reported strain (9, 17, 19). No other metabolite except 2-HBP was detected during the batch cultivation.
Although no desulfurization of DBT occurred after 70 h, cell
growth was sustained to 100 h as shown in Fig. 1. We tried to determine the concentrations of sulfate and sulfite by using a 2000i/sp
ion chromatograph (Dionex, Osaka, Japan), an IonPac AS4A anion-exchange
column with a cation suppressor, and a conductivity detector as
described by Omori et al. (17). The minimum detection limit
for this method was about 0.01 mM. However, no detectable level of
sulfate or sulfite accumulation in the broth was observed during the
cultivation of strain CYKS1. The amount of sulfur assimilated per gram
of DCW was about 0.11 mmol. If we consider that the sulfur content of
Escherichia coli, for example, is about 0.14 mmol/g of DCW
(2), it seems that all of the sulfur released from DBT was
assimilated by the cells. After about 70 h, cells might be sufficiently supplied with sulfur and sulfur would no longer be a
growth-limiting factor, making further DBT desulfurization unnecessary after this period of cultivation.
When sulfate was added to the MSM, DBT was not desulfurized, indicating
that sulfate completely repressed the expression of DBT-desulfurizing
activities as previously reported by Omori et al. (18).
Therefore, for the efficient desulfurization of fossil fuels, it would
be advantageous to develop new strains that are not susceptible to
sulfate repression (20).
Metabolic pathway and characteristics of DBT
desulfurization.
When cells were induced with DBT,
DBTO2 could be desulfurized to 2-HBP with no lag time. This
result implied that DBTO2 could be an intermediate of DBT
desulfurization. The specific rates of desulfurization of DBT and
DBTO2 by the resting cells were 8.9 and 17.9 µmol of
S · g (DCW)
1 · h1,
respectively. Because DBTO2-desulfurizing activity was
about two times higher than DBT-desulfurizing activity,
DBTO2 could not be accumulated during the DBT
desulfurization. When resting cells were prepared in a minimal medium
with a modified trace element solution (13), a
hydrophilic intermediate was accumulated during the DBT or
DBTO2 desulfurization. For the
characterization of the sulfur-containing metabolite, a
GC-sulfurchemiluminescence detector (SCD) (model 350; Sievers
Instruments, Boulder, Colo.) was used. GC-SCD data indicated that the
hydrophobic intermediate was a sulfur-containing compound. Since its
mass ions (at m/z 216) corresponded to those of the
dibenz[c,e][1,2]oxanthiin 6-oxide that was formed from the
esterification of 2-(2-hydroxyphenyl) benzenesulfinate (HPBS) at acidic
pH during its analysis as described by Gallagher et al. (6),
our data were consistent with it being HPBS. HPBS is known as an
intermediate detected during the desulfurization of DBT by the
Rhodococcus sp. strain IGTS8 (6, 7).
These results suggest that DBT was oxidized to DBTO2 and
then cleaved hydrolytically to form HPBS by strain CYKS1. Therefore,
the newly isolated strain, Gordona strain CYKS1, was
considered to desulfurize DBT to 2-HBP via the 4S pathway (7,
17) as shown in Fig. 2. Considering
that 2-HBP itself has valuable combustible compounds, strain CYKS1
could be a much more promising biocatalyst for the treatment of fuel
oils than other strains that use DBT as a carbon and energy source and
thus cause a fuel value loss (14, 23).
As previously suggested by the batch culture results, desulfurizing
activity was sensitive to the growth phase. To determine the
desulfurization activity of cells in different growth phases, we
cultivated strain CYKS1 under DBT-limited conditions of 0.1 mM DBT.
Cell growth was sustained for 10 h after the complete depletion of
DBT. However, during this late growth phase without DBT, the cell
showed significantly decreased specific desulfurization activity (about
0.3 µmol of S · g [DCW]1 · h1) relative to that of early growth phase. As described
above, this result indicated that the sulfur accumulated in the cells during DBT desulfurization might be used for late growth. Furthermore, we could not detect DBT desulfurization activity after the
early growth phase even in the presence of sufficient DBT, as shown in
the batch culture. From these results, we concluded that resting cells
of the wild-type strain of CYKS1 must be prepared at the early growth
phase when they are used for the desulfurization of fossil fuels.
Desulfurization of diesel oils.
There are some reports
concerning the microbial desulfurization of DBT as described above.
However, the treatment of fuel oils by desulfurizing microbial strains
is in its infant stage, with only a few articles published in this area
(11, 16, 24). Petroleum-based fuel oils including diesel
oils contain an enormous number of organic sulfur compounds, including
DBT. We investigated the capability of strain CYKS1 to (i) use organic
sulfur compounds other than DBT as a sole sulfur source, (ii)
desulfurize DBT in the organic rather than the aqueous phase, and (iii)
be used in treatment of two types of diesel fuels, middle distillate
unit feed (MDUF) and light gas oil (LGO).
We observed growth of strain CYKS1 on the organic sulfur compounds
listed in Table 1. The results showed
that strain CYKS1 could utilize various organic sulfur compounds which
are believed to exist in fuel oils, although the list in Table 1 did
not represent the full spectrum of sulfur compounds in fuel oils.
Without glucose in the medium, strain CYKS1 was unable to grow on any
of the compounds listed in Table 1 as a sole carbon source.
To study the capability of strain CYKS1 to desulfurize DBT in the
organic phase, we employed a two-phase system: cells in DBT-free MSM
and DBT in hexadecane, one of the major hydrocarbons in diesel oils.
Two milliliters of hexadecane containing 5 mM DBT was mixed with 18 ml
of inoculated MSM in 100-ml Erlenmeyer flasks and incubated in a
gyratory shaker at 30°C. Strain CYKS1 grew well in this two-phase
medium. The DBT concentration in hexadecane decreased from 5.0 to
approximately 2.2 mM in 48 h, and a stoichiometric amount of 2-HBP
was detected in the oil phase.
In the treatment of diesel oils, 1 ml of diesel oil was mixed with 9 ml
of a resting cell suspension in 25 mM phosphate buffer and added to
100-ml Erlenmeyer flasks. The cultures were incubated in a shaker at
170 rpm and 30°C for 12 h. After sampling, the separation of the
oil and cell suspension was done by centrifugation (15,000 × g, 20 min). To determine the total sulfur content of the
oil, the oil phase was injected directly into a GC-SCD (without extraction) as described previously (5, 11). The lower limit of detection of total sulfur by this method was about 50 ppm. These
data were confirmed by using a 7000S total sulfur analyzer (Antek
Instruments, Inc.) as described previously (11). Figure 3A shows GC-SCD peaks for all of the
sulfur compounds in the MDUF (with about 0.15% [wt/wt] sulfur
initially) before treatment. After treatment of the MDUF, all of the
peaks, including the one for DBT, significantly decreased in height as
shown in Fig. 3B. After treatment, only a small amount of sulfate,
equivalent to less than 30% of the sulfur removed from the oil, was
detected in the reaction mixtures. It is important to note that the
sulfur compounds with retention times longer than about 5 min nearly disappeared. Such characteristics of desulfurization by strain CYKS1
are opposite or complementary to those of hydrodesulfurization, in
which sulfur compounds with a shorter residence time are more easily
desulfurized (4). Based on these results, DBT-induced resting cells of strain CYKS1 are considered to have a sufficiently broad substrate specificity to desulfurize major organic sulfur compounds contained in diesel oils. Bacterial strains specifically cleaving the carbon-sulfur bonds like strain CYKS1 are more effective in the treatment of fuel oils than microorganisms using a
carbon-destructive pathway such as Brevibacterium
(23) or Pseudomonas (14), which might
have a limited range of substrates to be desulfurized.
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FIG. 3.
Desulfurization of MDUF by strain CYKS1. GC-SCD
chromatograms for MDUF before (A) and after (B) treatment are shown.
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|
Compared with those of DBT in the aqueous phase, the desulfurization
rates of diesel oils were observed to be much lower. The specific
desulfurization rates of MDUF and LGO were 5.3 and 4.7 µmol of S
· g (DCW)1 · h1, respectively. The
total sulfur content of MDUF decreased by about 70% (wt/wt) after
treatment. For LGO, which had an initial sulfur content of
approximately 0.3% (wt/wt), the total sulfur content decreased by
about 50%. Organic sulfur compounds detected as the baseline by the
GC-SCD could not be desulfurized by treatment with strain CYKS1.
As a conclusion, strain CYKS1 has a good potential for use in the
biocatalytic desulfurization of fuel oils.
| |
ACKNOWLEDGMENTS |
This work was supported by a grant from R & D Management
Center for Energy and Resources, as a part of the Clean Energy
Program.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: BioProcess
Engineering Research Center, Korea Advanced Institute of Science and
Technology, 373-1, Kusong-dong, Yusung-gu, Taejon 305-701, Korea.
Phone: 82 42 869 3927. Fax: 82 42 869 8800. E-mail:
ychang{at}sorak.kaist.ac.kr.
| |
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Appl Environ Microbiol, June 1998, p. 2327-2331, Vol. 64, No. 6
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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