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Appl Environ Microbiol, May 1998, p. 1884-1889, Vol. 64, No. 5
National Research Council,1 and
NHEERL, Gulf Ecology Division, U.S. Environmental Protection
Agency,2 Gulf Breeze, Florida 32561 and
Biochemistry Department, University of Minnesota, St. Paul,
Minnesota 551083
Received 16 September 1997/Accepted 20 January 1998
Aromatic compounds with alkyl substituents are abundant in fossil
fuels. These compounds become important environmental sources of
soluble toxic products, developmental inhibitors, etc. principally through biological activities. To assess the effect of methyl substitution on the completeness of mineralization and accumulation of
pathway products, an isolate from a phenanthrene enrichment culture,
Sphingomonas paucimobilis 2322, was used. Washed cell suspensions containing cells grown on 2,6-dimethylnaphthalene in
mineral medium were incubated with various mono-, di-, and trimethylnaphthalene isomers, and the products were identified and
quantified by gas chromatography and mass spectrometry. The data
revealed enzymes with relaxed substrate specificity that initiate
metabolism either by methyl group monoxygenation or by ring
dioxygenation. Congeners with a methyl group on each ring initially
hydroxylate a methyl, and this is followed by conversion to a carboxyl;
when there are two methyl groups on a single ring, the first reaction
is aryl dioxygenation of the unsubstituted ring. Intermediates are
channeled to primary ring fission via dihydrodiols to form
methyl-substituted salicylates. Further evidence that there are
multiple pathways comes from the fact that both phthalate and
(methyl)salicylate are formed from 2-methylnaphthalene.
Alkylated aromatic hydrocarbons
enter the ecosystem mostly from crude oil- and petroleum-derived
materials. Many of these compounds are man-made products of large-scale
industry and are used as fuels, solvents, detergent precursors, and
commercial insect repellents (for example, methylnaphthalenes dispersed
in aromatic solvents for mosquito control) (42, 47). Because of the abundance of methyl-substituted aromatic compounds and the
formation of water-soluble products, the effects of these compounds on
the biosphere may be greater than the toxic damage caused by the
unsubstituted hydrocarbon counterparts (1, 10, 19, 29, 30,
37).
Removal of aromatic compounds from the biosphere is principally a
microbial activity. Gibson et al. (20) first reported that
unsubstituted structures undergo initial ring reductive dioxygenation to cis-dihydrodiols. With ring substituents, the positions
exert a major effect on the first reaction site, the pathway, and the products. With a single methyl addition, ring dioxygenation may be
retained, or methyl monoxygenation may first form the analogous benzylic alcohol. The most extensive studies have examined toluene, the
simplest and most abundant methylated aromatic hydrocarbon. A recent
summary of six known schemes for toluene metabolic patterns are
reviewed in studies of fungal oxygenation (45). The products and genetics of both ring dioxygenation (the TOD pathway)
(48) and side chain monooxygenation (the TOL pathway)
(2) are well-documented. Data are also available for
representative aromatized plant terpenes and homologs, including
p-cymene (15), 3-ethyltoluene (28), and the xylene isomers (3, 16). The attention that has been devoted to methyl derivatives is limited (1, 5, 31, 39) compared with the attention that has been devoted to unsubstituted fused ring compounds (4, 9, 14, 27, 43). Moreover, although
a very large number of strains have been isolated, few organisms have
received the attention needed for even minimal biological and chemical
characterization, and fewer still have been subjected to a genetic
analysis to determine chromosome organization, regulation, and gene
origin. The detailed data available suggest there is a limited variety
of oxygenase catalytic centers in animal, plant, and microbial systems.
Marked similarities among mono- and dioxygenase systems have led to the
concept that there are enzyme superfamilies (36). Three
oxygenase centers that contain metal (iron) prosthetic groups have been
well-documented. The most abundant center, which was the first center
documented, is a unique heme-thiolate monoxygenase center which now
contains more that 500 related, but separate, protein sequences
(36). Two other well-studied oxygenase reaction centers are
the Fe2(µO)2 cluster, which was found first
in methane monoxygenase and later in related nonheme di-iron enzymes
(41), and disassociable ferrous, mononuclear nonheme iron
coordination sites (25). The essential two-electron reducing
power of both mono- and dioxygenase systems is provided primarily by
flavoprotein reductases; here too, a limited number of structural
patterns are found (17), and there is marked homology to the
anaplerotic heterotrophic and photosynthetic flavoproteins (6, 17,
22, 23, 32).
A variety of bacterial strains and species have been used to identify
products of methyl-substituted aromatic hydrocarbon metabolism. The
profiles obtained are the principal sources of deduced
oxygenation-oxidation patterns. Most previous studies on fused ring
alkyl aromatic compounds have been concerned with the 1- and
2-methylnaphthalenes and the isomer effects on initial methyl
monooxygenation (13, 31, 39, 46) compared with ring
dioxygenation (7, 8, 14, 44, 46). Pseudomonas putida CSV86, for example, has been reported to convert 1- and 2-methylnaphthalenes to the respective methyl catechols by ring dioxygenation or to form naphthoic acids following methyl hydroxylation (31). In addition, the 2-methyl isomer has been reported to yield 4-hydroxymethyl catechol (31), implying that there is dual-pathway regulation. In vitro eucaryote oxygenation has also been
found in hepatic microsomes (11, 26), fungi (13),
and cyanobacteria (12), the role in plant cells is unclear.
Data on fused ring dimethyl structures are more limited; thus, the
pathways are not understood as well (5, 21, 33). In early
studies Barnsley (5) and other workers identified ring
fission products obtained from fused ring aromatic compounds, and
subsequently the process was well-documented by Eaton and Chapman
(18). Barnsley (5) hypothesized that there is an initial 2-methyl hydroxylation, followed by oxidation to carboxylate and then a ring monohydroxylation to
1-hydroxy-6-methylnaphthalene-2-carboxylic acid. More recently, several
workers have described dioxygenation to 1-hydroxy-2-naphthoic acid as
an alternate product obtained from phenanthrene, 2-methylnaphthalene,
or 2-naphthoic acid (4, 5, 34). Workers have also described
methyl group oxidation of dimethylnaphthalene isomers by the
naphthalene dioxygenase cloned from plasmid NAH7 (40) and by
Nocardia corallina (Rhodococcus sp.) grown on
aliphatic hydrocarbons (24, 38).
In this report we describe the effect of methyl-substituted aromatic
isomers on the metabolic pathway(s) in washed cell suspensions of
Sphingomonas paucimobilis 2322 grown on
2,6-dimethylnaphthalene (2,6-DMN) as a carbon and energy source. Our
data documented that relaxed enzyme specificity and isomer substitution
effects on mineralization pathways occur.
Organism, cultures, chemicals, and products.
S.
paucimobilis 2322 from the collection of Peter Chapman (Gulf
Ecology Division, U.S. Environmental Protection Agency) was isolated
from a creosote-contaminated soil by enrichment on phenanthrene as the
carbon source. The biological systematic properties of this organism
were determined and fatty acid analyses and a 16S rRNA composition
analysis were performed by Midi Laboratories, Newark, Del. Cells were
grown in a liquid mineral salt medium (pH 7.0) containing (per liter)
3.24 g of K2HPO4, 0.87 g of
NaH2PO4, 2.0 g of NH4Cl, 123 mg of nitrilotriacetic acid, 200 mg of MgSO4 · 7H2O, 12 mg of FeSO4 · 7H2O,
3 mg of MnSO4 · H2O, 3 mg of
ZnSO4 · 7H2O, and 1 mg of
CoCl2 · 6H2O. Solid media contained 2%
agar (Difco). Cells were grown by incubating them at 30°C on a rotary shaker (180 rpm) in 2-liter Erlenmeyer flasks containing 400 ml of
mineral salt medium supplemented with 1 g of a carbon source per
liter. The cells were harvested from 48-h-old cultures by centrifugation (8,000 × g, 10 min), washed twice by
suspending them in a volume equal to 1/10th the growth volume,
collected by centrifugation, and resuspended (final volume, 100 ml) to
an optical density at 600 nm of 2.0. For fermentation studies a
hydrocarbon was added to a concentration of 1 g/liter to washed cell
suspensions in individual Erlenmeyer flasks, and the flasks were
incubated at 30°C for up to 72 h. After incubation, cells (and
undissolved substrate, when present) were removed by centrifugation,
and the supernatants were acidified to pH 2 to 3 with concentrated
hydrochloric acid and extracted twice with equal volumes of ethyl
acetate. The extracts were dried over anhydrous sodium sulfate and
evaporated under reduced pressure at 30°C, and the materials
recovered were methylated with an ethereal solution of diazomethane
prior to gas chromatography-mass spectrometry (GC-MS) analysis. All
chemicals were of the highest purity commercially available.
Analyses.
GC-MS was performed with a Hewlett-Packard model
5890 series II gas chromatograph equipped with a model HP5971
mass-selective detector and a model HP 5965B infrared detector.
Compounds were separated on a type HP-5 capillary column (25 m by 0.32 mm; film thickness, 0.25 µm) by using helium as the carrier gas at a
flow rate of 23 cm/s. The column temperature was kept isothermally at
50°C for 1 min and then increased to 290°C at a rate of 5°C/min. The mass spectrometer was operated at an electron ionization energy of
70 eV, and the injector, transfer line, and analyzer temperatures were
150, 300, and 300°C, respectively. Instrumental library searches and
comparison with available authentic compounds were used to identify
possible metabolites. The relative amounts of metabolites were
calculated from the peak areas of GC-MS total ion current chromatograms. The total ion current integrated responses (excluding the peak of residual starting material) were used as 100% internal standard values for each sample analyzed. Parallel processes without substrate were also included. Thin-layer chromatography was performed on 0.25-mm-thick silica gel (Merck Silica Gel 60 F254) plates by using
methylene chloride-ethyl acetate (1:1) as the developing solvent, and
the results were used for preliminary identification. Starting
substrates and metabolites were detected under UV light and by exposure
to iodine vapor. All of the chemicals used were of the highest purity
available commercially, and identities were confirmed by GC-MS
analysis.
Culture growth.
It was shown previously that S. paucimobilis 2322 grows well aerobically on several aromatic
compounds, including 2,6-DMN, biphenyl, o-xylene,
p-cymene, and acenaphthene, as well as phenanthrene (13a). To confirm that there are a number of growth
substrates in the catabolic module, several compounds were tested, as
shown in Fig. 1. As discussed below a
number of related structures failed to support growth. With 2,6-DMN
yellow metabolites were present in culture filtrates.
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Oxidation of Methyl-Substituted Naphthalenes:
Pathways in a Versatile Sphingomonas paucimobilis
Strain
and
ABSTRACT
Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
RESULTS AND DISCUSSION
Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
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FIG. 1.
Growth of S. paucimobilis 2322 in minimal
salt medium containing aromatic compounds as carbon and energy sources.
2,3,6-DMN, 2,3,6-trimethylnaphthalene; Phn, phenanthrene.
Metabolic pathway with 2,6-DMN. Harvested and washed cell suspensions oxidized a variety of methylnaphthalenes whose metabolites, as detected by thin layer chromatography, were later identified; the levels of these metabolites were determined by GC-MS, as shown in Table 1. The initial methyl group oxidation, a common event with the isomers tested, led to the proposed metabolic patterns shown in Fig. 2.
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2,7-, 1,5-, 1,6-, and 1,8-DMNs. The reactions of 2,7-DMN were similar to the reactions of the 2,6-DMN isomer, as indicated by the presence of 2-hydroxymethyl-7-methylnaphthalene, 7-methyl-2-naphthoic acid, 1,2-dihydroxy-1-hydro-7-methyl-2-naphthoate, and 4-methylsalicylate (Table 1 and Fig. 2); the data indicate that there was dioxygenation at the 1,2 positions, forming 6- and 7-methyl-2-naphthoates. These are characteristic fission products found in the benzoate-toluate pattern (35).
The 1,5-, 1,6-, and 1,8-DMN isomers gave analogous methylnaphthoate and methylsalicylate accumulations. When 1,6-DMN was used, GC-MS analysis revealed both 5- and 6-methylsalicylates (i.e., hydroxylation occurred at either the
-methyl group or the -methyl group). The 1,8-DMN
isomer products were "upper-pathway" products (i.e.,
1-hydroxymethyl-8-methylnaphthalene, 8-methyl-1-naphthaldehyde, and
1,8-naphthalide, a spontaneously cyclized product of
8-hydroxymethyl-1-naphthoic acid obtained under acidic extraction
conditions) (40).
2,3,6-Trimethylnaphthalene.
With methyl groups on both rings
and a third substituent at position 3
, methyl hydroxylation occurred
as the first committed step, at either carbon 2 or carbon 6,
and oxidation to the carboxylate led to compounds 27 and 28 (the
3,6-dimethyl- and 6,7-dimethyl-2-naphthoates) (Table 1). The subsequent
ring dioxygenation, however, appeared to be specific for the
(renumbered) 2,3-dimethyl-6-naphthoate, for only
4,5-dimethylsalicylate was present. The S. paucimobilis products obtained from 2,3,6-trimethylnaphthalene are consistent with
dioxygenation of the benzoate-toluate type (35).
1,2-, 1,4-, and 2,3-DMNs. As indicated above, placing both methyl groups on the same carbocyclic ring directed the initial reaction to dioxygenation of the unsubstituted aryl group and altered the early products. A subsequent meta ring fission should then have led to the respective dimethylsalicylates (that is, the 1,2-, 1,4-, and 2,3-DMNs and conversion to the respective 3,4-, 3,6-, and 4,5-dimethylsalicylic acids). The final products obtained from the salicylic acids converged regardless of whether one or both aryl ring substitutions occurred. An alternate oxidation, to the benzyl alcohols, yielded the apparent dead end compounds 23, 12, and 25, for neither salicylate nor phthalate derivatives were detected in the spent growth medium or after reactions with cell suspensions. The data are compatible with the presence of the phenanthrene dioxygenase, which apparently is coinduced in cells grown with 2,6-DMN.
2-Methylnaphthalene. 2-Methylnaphthalene, although not a growth substrate, was metabolized by washed cells grown on 2,6-DMN. The products indicate that initially either methyl hydroxylation or dioxygenation of an unsubstituted aryl ring occur. Thus, ring fission led to either 4-methylsalicylate or phthalate. Figure 2 shows the same dual pathways found in phenanthrene-grown cells.
Dioxygenation initiated on the unsubstituted aryl ring occurred by formation of a cis-dihydrodiol at the 1,2 carbons. As indicated in Fig. 2, the data suggest that dehydrogenation to the analogous vicinal 1,2-diphenol (a catechol) and ring fission to 4-methylsalicylate via compound 37 or 38 (2-hydroxy-7-methylchromene-2-carboxylate or trans-2-hydroxy-4-methylbenzylidinepyruvate) occur. A GC-MS analysis of the methylated product revealed a relative amount of 6% (GC Rt = 16.71 min; MS m/z [%]: 234 [M+] [4], 219 [1], 203 [6], 187 [14], 175 [100], 160 [1], 159 [5], 143 [6], 132 [12], 115 [19]). A-methyl hydroxylation first led to phthalate or salicylate,
depending on the reaction of compound 33. The presence of 2-naphthoate and 1-hydroxy-2-naphthoate recalls the Bradley monoxygenase hypothesis (5). When 2-naphthoate (compound 32) was used as the
substrate, the products indicated that both mono- and dioxygenase
pathways were present, based on identification of compounds 33 and 34, which led to phthalate (compound 31) or 4-methylsalicylate (compound 30). Phthalate generation from 1-hydroxy-2-naphthoate and 2-naphthoate is a well-established pathway in phenanthrene metabolism (4, 34).
To summarize, S. paucimobilis grown on phenanthrene
generates phthalate via 1-hydroxy-2-naphthoate and salicylate in trace amounts in spent growth medium and washed cell suspensions. Thus, although the phenanthrene and 2,6-DMN pathways are considered separate,
the two pathways seem to be coinduced by growth on either substrate,
suggesting that there is a common regulation mechanism.
A comment on the growth substrates of strain 2322 is in order. In
general, the 2-substituted dimethylnaphthalene isomers are suitable
growth substrates, as are the 2,3,6-trimethyl structure and
phenanthrene. Naphthalene and mono-substituted 2-naphthalenes, however,
do not support growth. Similarly, in strains of this type, neither
1-substituted dimethylnaphthalenes nor 1- or 2-naphthoate supports
growth. The persistence of these compounds in nature requires more
detailed consideration, along with the effects of other microbic
strains (31), but this was beyond the scope of this work.
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ACKNOWLEDGMENTS |
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This work was supported in part by a National Research Council Resident Research Associateship Award (to T.K.D.) and by cooperative agreement CR823946-01-0 with the U.S. Environmental Protection Agency (to S.A.S.).
We thank Maureen Downey (Avanti Corporation) for carrying out GC-MS analyses. We also thank Peter J. Chapman for supplying strain 2322, for making reference chemicals available, and for helpful discussions. We are grateful to Peter J. Chapman for reviewing the manuscript and making insightful suggestions.
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FOOTNOTES |
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* Corresponding author. Mailing address: NHEERL, GED, U.S. EPA, 1 Sabine Island Drive, Gulf Breeze, FL 32561. Phone: (850) 934-2497. Fax: (850) 934-9201. E-mail: dutta.tapan{at}epamail.epa.gov/gunny{at}gulf.net.
Contribution 1024 from the NHEERL, Gulf Ecology Division,
U.S. Environmental Protection Agency, Gulf Breeze, Fla.
Present address: Maxygen, Inc., Santa Clara, CA 95051.
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Abstract
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Materials & Methods
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References
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Appl Environ Microbiol, May 1998, p. 1884-1889, Vol. 64, No. 5
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