RESEARCH LETTER
Sulfoquinovose degraded by pure cultures of bacteria with
release of C3-organosulfonates: complete degradation in
two-member communities
Karin Denger1, Thomas Huhn2, Klaus Hollemeyer3, David Schleheck1 & Alasdair M. Cook1
1
Department of Biology, University of Konstanz, Konstanz, Germany; 2Department of Chemistry, University of Konstanz, Konstanz, Germany; and
Institute of Biochemical Engineering, University of the Saarland, Saarbrücken, Germany
3
Correspondence: Alasdair M. Cook,
Department of Biology, University of
Konstanz, D-78457 Konstanz, Germany. Tel.:
+49 753 188 4247; fax: +49 753 188 2966;
e-mail: [email protected]
Received 14 October 2011; revised 28
November 2011; accepted 28 November
2011.
Final version published online 11 January
2012.
DOI: 10.1111/j.1574-6968.2011.02477.x
MICROBIOLOGY LETTERS
Editor: Christiane Dahl
Keywords
Cupriavidus pinatubonensis;
dihydroxypropanesulfonate; Klebsiella
oxytoca; Paracoccus pantotrophus;
Pseudomonas putida; 3-sulfolactate.
Abstract
Sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) was synthesized chemically. An
HPLC-ELSD method to separate SQ and other chromophore-free sulfonates,
e.g. 2,3-dihydroxypropane-1-sulfonate (DHPS), was developed. A set of 10
genome-sequenced, sulfonate-utilizing bacteria did not utilize SQ, but an isolate, Pseudomonas putida SQ1, from an enrichment culture did so. The molar
growth yield with SQ was half of that with glucose, and 1 mol 3-sulfolactate
(mol SQ) 1 was formed during growth. The 3-sulfolactate was degraded by
the addition of Paracoccus pantotrophus NKNCYSA, and the sulfonate sulfur
was recovered quantitatively as sulfate. Another isolate, Klebsiella oxytoca
TauN1, could utilize SQ, forming 1 mol DHPS (mol SQ) 1; the molar growth
yield with SQ was half of that with glucose. This DHPS could be degraded by
Cupriavidus pinatubonensis JMP134, with quantitative recovery of the sulfonate
sulfur as sulfate. We presume that SQ can be degraded by communities in the
environment.
Introduction
Sulfoquinovose (SQ; 6-deoxy-6-sulfoglucose) (Fig. 1) is
the polar head group of the plant sulfolipid (Benson,
1963), the annual production of SQ by phototrophs is
about 10 000 000 000 tonnes (Harwood & Nicholls,
1979), and very little is known about its biodegradation.
Bacteria from the Americas degrade SQ quantitatively to
sulfate and cell material via intracellular cysteate and sulfoacetate (Martelli & Benson, 1964; Martelli & Souza,
1970), but these organisms were lost (Cook & Denger,
2002). All five SQ-degrading bacteria from Europe,
including a strain of Pseudomonas putida, released substoichiometric amounts of sulfate from SQ (Roy et al.,
2000, 2003). Two organisms (e.g. Pseudomonas sp. and
Klebsiella sp. strain ABR11) excreted organosulfonates
(and, e.g. acetate), which were identified in the medium
by C13-NMR as 3-sulfolactate and 2,3-dihydroxypropane1-sulfonate (DHPS, sulfopropanediol) (Roy et al., 2003)
FEMS Microbiol Lett 328 (2012) 39–45
(chemical structures in Fig. 1). Two organisms expressed
phosphofructokinase, consistent with the operation of a
glycolytic-type degradative pathway for SQ. Klebsiella sp.
strain ABR11 also expressed an NAD+-dependent SQdehydrogenase activity (Roy et al., 2003).
More recently, organisms able to utilize sulfolactate
and/or DHPS have been discovered, and corresponding
degradative pathways elucidated (e.g. Denger & Cook,
2010; Mayer et al., 2010). Further, sulfonate excretion
systems in degradative pathways have been proposed
(e.g. Weinitschke et al., 2007; Mayer & Cook, 2009;
Krejčı́k et al., 2010).
We wanted to use genome-sequenced organisms to
expand on the work of Roy et al. (2000, 2003), but had
little success with this approach, so we isolated an organism
able to utilize SQ as a sole source of carbon and energy for
growth. It was identified as a strain of P. putida, as found
earlier by Roy et al. (2000), so we followed their lead to
Klebsiella sp. and found that our sulfonate-utilizing
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Published by Blackwell Publishing Ltd. All rights reserved
40
K. Denger et al.
Growth of
Pseudomonas putida SQ1
Growth of
Paracoccus pantotrophus NKNCYSA
O
–
SO3
SO3
OH
–
3-sulfolactate
(Slac)
O
HO
SO42–
–
O
HO
OH
OH
Sulfoquinovose
(SQ)
Growth of
Klebsiella oxytoca TauN1
Growth of
Cupriavidus pinatubonensis JMP134
–
SO3
HO
OH
SO42–
2,3-dihydroxypropane-1-sulfonate
(DHPS)
Fig. 1. Sulfoquinovose degraded by two pure cultures to 3-sulfolactate or DHPS, and the degradation of these two compounds by two SQnegative pure cultures to yield sulfate stoichiometrically.
Klebsiella oxytoca TauN1 (Styp von Rekowski et al., 2005)
also utilized SQ. Each organism excreted a C3-sulfonate,
which could be completely degraded by a second bacterium.
Materials and methods
Chemical syntheses
Synthesis of SQ was achieved following in part the protocols of Miyano & Benson (1962) and of Roy & Hewlins
(1997) without the need to form its barium salt for purification. The starting material for the preparation of SQ,
1,2-O-isopropylidene-6-O-tosyl-D-glucofuranose was prepared from 1,2-O-isopropylidene-D-glucofuranose by
tosylation (Valverde et al., 1987) and isolated chromatographically pure. The tosylate (2.0 g) dissolved in ethanol
(20 mL) was refluxed with an aqueous solution of
Na2SO3 (1.21 g in 20 mL) under an inert gas atmosphere.
Complete consumption of the starting tosyl compound
(Rf: 0.62) was detected after 24 h by TLC in ethyl acetate
on silica gel. Excess sodium sulfite was dissolved by the
addition of water (50 mL) and the ethanol removed
in vacuo. The aqueous solution was freed from sodium
ions by passing it through a strongly acidic Amberlite IR
120 ion exchange column (45 g). Concentration of the
acidic eluate under reduced pressure removed sulfur
dioxide and cleaved the isopropylidene protecting group,
leaving behind a syrup that consisted of equimolar
amounts of p–toluenesulfonic acid and 6-sulfo-D-quinovose.
Drying was continued at the lower pressure of an oil rotary
vane pump upon which the syrup became gum-like.
This gum was triturated with methanol upon which it
partly solidified. Decanting off the methanol and repeating the procedure with fresh methanol led finally to a
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complete solidification. The 1H-NMR spectrum, analogous to that of Roy & Hewlins (1997), showed an enrichment of SQ as a mixture of its anomers over
p-toluenesulfonic acid ( 10%) and no other organic
impurities. Data from MALDI-TOF-MS in the negative
ion mode gave m/z = 443 = [M 1] 1, which is consistent
with SQ (M = 444).
The syntheses of DHPS and racemic sulfolactate were
described elsewhere (Roy et al., 2003; Mayer et al., 2010).
Other chemicals were available commercially from SigmaAldrich, Fluka, Merck or Biomol.
Bacteria and growth conditions
Burkholderia phymatum STM815 (DSM 17167) (e.g. Elliott et al., 2007), Burkholderia xenovorans LB400 (e.g.
Chain et al., 2006), Cupriavidus necator H16 (DSM 428)
(e.g. Pohlmann et al., 2006), Cupriavidus pinatubonensis
JMP134 (DSM 4058) (Sato et al., 2006), K. oxytoca
TauN1 (DSM 16963) (Styp von Rekowski et al., 2005),
Paracoccus pantotrophus NKNCYSA (DSM 12449) (e.g.
Rein et al., 2005), Sinorhizobium meliloti Rm1021 (e.g.
Finan et al., 2001), Rhodopseudomonas palustris CGA009
(e.g. Larimer et al., 2004), Rhodobacter sphaeroides 2.4.1
(e.g. Mackenzie et al., 2001), P. putida F1 (e.g. Zylstra &
Gibson, 1989), and P. putida KT2440 (e.g. Nelson et al.,
2002) were grown aerobically at 30 °C in a phosphatebuffered mineral salts medium, pH 7.2 (Thurnheer et al.,
1986). Roseobacter litoralis Och 149 (DSM 6996) (e.g.
Kalhoefer et al., 2011) and Roseovarius sp. strain 217
(Schäfer et al., 2005) were cultured in a Tris-buffered
artificial seawater medium (Krejčı́k et al., 2008). Strain
Och 149 was grown at 25 °C and strain 217 required the
addition of vitamins (Pfennig, 1978). Roseovarius nubinhibens ISM (González et al., 2003) was grown in modified
FEMS Microbiol Lett 328 (2012) 39–45
41
Sulfoquinovose degraded in defined communities
Analytical methods
Growth was measured as turbidity at 580 nm and correlated with protein that was quantified in a Lowry-type
reaction (Cook & Hütter, 1981). Sulfate was quantified
turbidimetrically as a suspension of BaSO4 (Sörbo, 1987).
3-Sulfolactate was quantified by ion chromatography (IC)
with the conditions described for sulfoacetate (Denger
et al., 2004). DHPS was assayed qualitatively by the reaction of DHPS dehydrogenase [HpsN (EC 1.1.1.308) catalyzes the NAD+-dependent oxidation of DHPS to
sulfolactate] from the soluble fraction of C. pinatubonensis JMP134 (Mayer et al., 2010). The reaction mixture
contained in 50 mM Tris/HCl, pH 9.0, 2 mM NAD+, soluble fraction (about 0.3 mg protein mL 1) and outgrown
medium of K. oxytoca TauN1 after growth with sulfoquinovose. Standard methods were used for the Gram reaction and to assay catalase or cytochrome c-oxidase
activity (Gerhardt et al., 1994).
SQ was assayed with a colorimetric assay for reducing
sugars (2,3-dinitrosalicylic acid method; Sturgeon, 1990).
SQ was quantified by HPLC after separation on a Nucleodur HILIC (hydrophylic-interaction liquid chromatography) column (125 9 3 mm) (Macherey-Nagel, Düren,
Germany) and evaporative light-scattering detection
(ELSD). The isocratic eluent was 0.1 M ammonium acetate
in 80 % acetonitrile with a flow rate of 0.5 mL min 1.
Samples were dissolved in the eluent. Under those
conditions, DHPS, taurine (2-aminoethanesulfonate), and
glucose could also be analyzed directly in culture medium,
which did not interfere with the analyses (Fig. 2); sulfolacFEMS Microbiol Lett 328 (2012) 39–45
1.0
Chloride
Intensity (V)
Silicibacter basal medium (Denger et al., 2006) and
needed a supplement of 0.05% yeast extract (Denger
et al., 2009).
The sole carbon source was 5 mM sulfoquinovose or as
a control 20 mM acetate or taurine or 10 mM succinate
or 5 mM 4-toluenesulfonate or 5 mM glucose. Cultures
on the 3-mL scale in 30-mL screw-cap tubes were incubated in a roller. For growth experiments, 12-mL cultures
were grown in a beaker on a shaker, and 0.8 mL samples
were taken at intervals to measure the optical density at
580 nm and to analyze concentrations of substrate and
product.
Enrichment cultures were set up in a 3-mL scale in the
freshwater mineral salts medium with 5 mM SQ as sole
added carbon source. If turbidity developed and bacteria
could be seen under the microscope, subcultures in fresh
selective medium were inoculated. After four or five
transfers, cultures were streaked on LB-agar plates and
colonies were picked into fresh selective medium. After
three rounds of plating and picking from homogeneous
plates, cultures were considered pure.
0.5
DHPS
SQ
Glucose
Taurine
Injection
0
2
4
6
Retention time (min)
8
10
Fig. 2. HPLC-chromatogram showing separation of three sulfonates
and glucose when using a HILIC column and an ELSD detector. The
chloride is from the culture medium.
tate could also be quantified, but it interfered with the peak
of sulfoquinovose.
Results
Problems with the syntheses of SQ
The chemical synthesis of SQ is simple: two hydroxyl
groups of glucose are protected, and the hydroxyl group
at C-6 tosylated and the tosyl group are displaced by
sulfite. This yields two organic products, SQ and 4-toluenesulfonate, and, finally, sodium sulfate. The problem is
to separate the two organic products, in which we were
not fully successful. The consequence was that all organisms, with which we worked, had to be checked for
growth with 4-toluenesulfonate. No organism used in the
work utilized (or was inhibited by) 4-toluenesulfonate.
Separation and determination of SQ and its
metabolites
We initially assayed SQ, a reducing sugar, with a standard
method (Sturgeon, 1990) (e.g. Fig. 3). At low concentrations of sugar, the standard curve is, indeed, a curve and
the interpolation had to be made manually. We required
a different method, IC, for the metabolic product, 3-sulfolactate (Fig. 3), which eluted on the tail of the peak for
sulfate (not shown). These methods were just adequate
(Fig. 3), but inadequate for the next product, DHPS,
which we could not detect by IC.
What was needed was a detector which was sensitive
for nonchromophores and a column which could separate highly polar compounds. The ELSD detector and the
HILIC column met our demands (Fig. 2). We optimized
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Published by Blackwell Publishing Ltd. All rights reserved
42
K. Denger et al.
(b)
(a)
4
0.5
Concentration (mM)
Optical density at 580 nm
0.6
0.4
0.3
0.2
3
2
1
0.1
0
0.0
0
3
6
Time (h)
9
12
0.0
0.1
0.2
0.3
Optical density at 580 nm
the system for our purposes and had linear standard
curves between 0 and 5 pmol per injection (R2 > 0.99);
a fresh standard curve was needed with each set of
experiments.
Genome-sequenced organisms
We tested ten genome-sequenced organisms, which could
utilize C2- or C3-sulfonates within 1 week as sole carbon
and energy sources, for the ability to degrade SQ. No
candidate was detected. The organisms were the Alphaproteobacteria R. sphaeroides 2.4.1, R. palustris CGA009,
R. litoralis Och 149, R. nubinhibens ISM, Roseovarius sp.
strain 217, and S. meliloti Rm1021, and the Betaproteobacteria B. phymatum STM815, B. xenovorans LB400,
C. necator H16, and C. pinatubonensis JMP134.
Enrichment cultures
A set of aerobic enrichment cultures in SQ-mineral salts
medium with an inoculum from forest soil, sediment
from a forest pond or littoral sediment from Lake Constance yielded at least one positive culture per inoculum.
One representative, rapidly growing, pure culture, strain
SQ1 from the littoral sediment, was chosen for further
work because it grew homogeneously in suspended
culture. Its molar growth yield with SQ was half of that
with glucose (Fig. 3a). The organism was identified as
P. putida SQ1 by its 16S rRNA gene sequence and by its
physiology (Holt et al., 1994): a rod-shaped, motile,
nonspore-forming, Gram negative, catalase- and oxidasepositive aerobic bacterium.
Growth physiology of P. putida SQ1
Pseudomonas putida SQ1 grew in glucose salts medium
with a molar growth yield of 5.0 g protein (mol C) 1
(Fig. 3a), a value which indicated complete utilization of
the carbon source (Cook, 1987); glucose, measured as
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0.4
Fig. 3. Growth of Pseudomonas putida SQ1:
(a) growth with 4 mM glucose ( ) or 4 mM
sulfoquinovose ( ) and (b) concentrations of
sulfoquinovose ( ) and of sulfolactate (▲) as
a function of growth.
○
△
□
reducing sugar, disappeared. The organism grew only half
as much in equimolar SQ-salts medium (Fig. 3a). Analysis of the spent growth medium showed that the SQ had
disappeared completely, measured as reducing sugar, and
that a product was visible by IC. This product co-eluted
with authentic 3-sulfolactate and 1 mol sulfolactate
(mol SQ) 1 was formed (Fig. 3b). The identity of this
tentative 3-sulfolactate was confirmed by MALDI-TOFMS in the negative ion mode. A novel signal at m/z = 169 =
[M 1] 1 was found after growth, which corresponded to
the Mcalcd = 170 for 3-sulfolactate. After growth of
P. putida SQ1, we inoculated the outgrown medium with
P. pantotrophus NKNCYSA, a freshwater bacterium from
our culture collection known to degrade sulfolactate (Rein
et al., 2005) and which did not utilize SQ. Strain NKNCYSA grew, sulfolactate was degraded, and stoichiometric
amounts of sulfate were excreted into the medium (not
shown). There was mass balance for the conversion of SQ
to bacterial biomass and sulfate.
We had two genome-sequenced strains (F1 and
KT2440) of P. putida in our strain collection, but neither
organism utilized SQ, so we altered our strategy and used
nonsequenced organism(s).
Organisms found in recent work
An isolate of Klebsiella sp., strain ABR11, was found to utilize SQ and to excrete DHPS (Roy et al., 2003). So, we tried
a sulfonate-utilizing organism from our strain collection,
K. oxytoca TauN1, whose genome is not sequenced (Styp
von Rekowski et al., 2005) but which represents the genus
of Klebsiella sp. strain ABR11.
Klebsiella oxytoca TauN1 grew overnight with SQ as
sole source of carbon and energy, during which SQ disappeared (Fig. 4) and a compound was formed which
could be oxidized with soluble fraction of C. pinatubonensis JMP134 plus NAD+ by the reaction of DHPS dehydrogenase, HpsN. The growth yield with SQ was half of
that with glucose (not shown), consistent with excretion
FEMS Microbiol Lett 328 (2012) 39–45
43
Sulfoquinovose degraded in defined communities
Strain TauN1
+ strain JMP134
Concentration (mM)
5
4
3
2
1
0
0.0
0.2
0.4
0.4
Growth (OD580 nm)
0.6
0.8
□
Fig. 4. Degradation of 4 mM sulfoquinovose ( ) and formation of
dihydroxypropanesulfonate (▼) by Klebsiella oxytoca TauN1. After
growth of strain TauN1, Cupriavidus pinatubonensis JMP134 was
added, which degraded DHPS to sulfate ( ) and cell material. Further
explanation is given in the Results section.
•
of 1 mol DHPS (mol SQ) 1, which was supported by
HPLC (Fig. 4). These tentative identifications of DHPS
were confirmed by MALDI-TOF-MS in the negative ion
mode: A novel signal, which developed during growth,
m/z = 155 = [M 1] 1, matched the Mcalcd = 156 for
DHPS. Addition of the DHPS utilizer, C. pinatubonensis
JMP134, to outgrown K. oxytoca TauN1 medium allowed
growth (Fig. 4), and the DHPS disappeared while
equimolar sulfate was released into the medium. As with
P. putida SQ1 and P. pantotrophus NKNCYSA, there was
mass balance for the conversion of SQ to bacterial biomass and sulfate.
Discussion
The ease with which Martelli (in North and South America) (Martelli & Benson, 1964; Martelli, 1967; Martelli &
Souza, 1970) and Roy et al. (2000) (on a European island)
obtained bacteria able to utilize SQ was expanded on by
our positive enrichment cultures on the European mainland. The American isolates, where studied (Martelli &
Benson, 1964; Martelli & Souza, 1970), did not involve an
excreted intermediate, whereas all of the seven European
isolates (this paper and Roy et al., 2000, 2003) did so. The
excreted intermediates were 3-sulfolactate, recovered quantitatively (Fig. 3), and DHPS, which was also recovered
quantitatively (Fig. 4) (cf. Roy et al., 2003). These compounds are widespread, as are degradative organisms (see
Introduction) which can degrade them in co-culture (e.g.
Fig. 4). So, we presume SQ degradation in the environment to take place in communities (Fig. 4) that presumably include organisms of the type examined by Martelli
(Martelli & Benson, 1964; Martelli & Souza, 1970).
FEMS Microbiol Lett 328 (2012) 39–45
Our data make clear that the advances made by Roy
et al. (2003) are one key to understanding sulfoglycolysis
at the molecular basis. They anticipate sulfoglycolysis
(cleavage of 6-deoxy-6-sulfofructose-1-phosphate by an
aldolase) on the one hand and an Entner-Doudoroff-type
(or pentose-phosphate-type) pathway (oxidation of SQ to
the lactone) on the other.
We anticipated rapid access to genome-sequenced
SQ degraders, to allow rapid identification of genes, e.g.
via peptide-mass fingerprint, and then pathways (e.g.
Mayer et al., 2010). But neither our screen of genomesequenced sulfonate utilizers nor our change from wildtype P. putida SQ to genome-sequenced P. putida spp.
brought success, though we still believe in this approach.
Acknowledgements
The project was supported by the University of Konstanz
and by the German Research Foundation (DFG) (SCHL
1936/1-1 to DS).
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