inducible uptake and metabolism of glucose by the phosphorylative pathway in pseudomonas putida...

Inducible uptakeandmetabolismofglucoseby thephosphorylativepathway in Pseudomonas putida CSV86Aditya Basu & Prashant S. Phale

Biotechnology group, School of Biosciences and Bioengineering, Indian Institute of Technology-Bombay, Powai, Mumbai, India

Correspondence: Prashant S. Phale,

Biotechnology Group, School of Biosciences

and Bioengineering, Indian Institute of

Technology-Bombay, Powai, Mumbai 400

076, India. Tel.: 191 22 25767836; fax: 191

22 25723480; e-mail: [email protected]

Received 28 January 2006; revised 19 April

2006; accepted 20 April 2006.

First published online May 2006.

doi:10.1111/j.1574-6968.2006.00285.x

Editor: Wilfrid Mitchell

Keywords

Pseudomonas ; glucose metabolism; transport;

enzyme induction; aromatic compound

catabolism.

Abstract

Pseudomonas putida CSV86 utilizes glucose, naphthalene, methylnaphthalene,

benzyl alcohol and benzoate as the sole source of carbon and energy. Compared

with glucose, cells grew faster on aromatic compounds as well as on organic acids.

The organism failed to grow on gluconate, 2-ketogluconate, fructose and manni-

tol. Whole-cell oxygen uptake, enzyme activity and metabolic studies suggest that

in strain CSV86 glucose utilization is exclusively by the intracellular phosphor-

ylative pathway, while in Stenotrophomonas maltophilia CSV89 and P. putida

KT2442 glucose is metabolized by both direct oxidative and indirect phosphor-

ylative pathways. Cells grown on glucose showed five- to sixfold higher activity of

glucose-6-phosphate dehydrogenase compared with cells grown on aromatic

compounds or organic acids as the carbon source. Study of [14C]glucose uptake

by whole cells indicates that the glucose is taken up by active transport. Metabolic

and transport studies clearly demonstrate that glucose metabolism is suppressed

when strain CSV86 is grown on aromatic compounds or organic acids.

Introduction

A variety of aromatic compounds are present in fresh and

marine waters and in agricultural lands. The most effective

and economical way to remove these compounds from the

environment is by microbial degradation (Alexander, 1981).

The bottleneck in the efficient degradation of these com-

pounds is the presence of simple carbon sources like organic

acids and sugars, which are preferentially utilized by micro-

organisms, and unless the simpler carbon sources are

completely depleted, the toxic aromatic compounds are not

degraded (Collier et al., 1996). In pseudomonads, glucose

utilization follows two routes: (i) the direct oxidative path-

way, which converts glucose to gluconate, 2-ketogluconate

and then subsequently to 6-phosphogluconate by extracel-

lular, high affinity, glucose dehydrogenase and gluconate

dehydrogenase (Quay et al., 1972; Midgley & Dawes, 1973;

Roberts et al., 1973; Lessie et al., 1979), and (ii) the

intracellular, low affinity, nucleotide-dependent phosphor-

ylative pathway (Lessie & Neidhardt, 1967; Tiwari & Camp-

bell, 1969; Eisenberg et al., 1974; Guymon & Eagon, 1974)

wherein glucose is converted to 6-phosphogluoconate by

glucokinase and glucose 6-phosphate dehydrogenase (Zwf).

The key intermediate for both pathways is 6-phosphogluco-

nate, which enters the TCA cycle via glyceraldehyde-3-

phosphate and pyruvate through the Entner-Doudoroff

pathway (Fig. 1a) (Entner & Doudoroff, 1952; Tiwari &

Campbell, 1969). Depending on the physiological condi-

tions, one or other of the pathways predominates (Lessie &

Phibbs, 1984).

It has been reported that degradation of aromatic com-

pounds is repressed by glucose as well as by organic acids

(Worsey & Williams, 1975; Duetz et al., 1994; Holtel et al.,

1994; Schleissner et al., 1994; Muller et al., 1996, 1997;

McFall et al., 1997). Such preferential utilization of simple

carbon sources represses degradation of recalcitrant com-

pounds in nature (referred to as carbon catabolite repres-

sion). Attempts have been made to overcome this repression

by generating mutants defective in glucose utilization which

will mineralize complex carbon sources like naphthalene

efficiently even in the presence of glucose (Samanta et al.,

2001).

Pseudomonas putida CSV86 has been shown to metabo-

lize aromatic compounds preferentially over glucose and

cometabolize aromatic compounds and organic acids (Basu

et al., 2006). Here we report that strain CSV86 utilizes

glucose only by the intracellular, phosphorylative pathway.

The strain utilizes aromatic compounds and organic acids

faster compared with glucose, and the glucose-metabolizing

FEMS Microbiol Lett 259 (2006) 311–316 c� 2006 Federation of European Microbiological SocietiesPublished by Blackwell Publishing Ltd. All rights reserved

enzyme, Zwf, and glucose transport are inducible and

suppressed by growth on aromatics or organic acids.

Materials and methods

Growth conditions

Bacterial cultures used in this study were P. putida CSV86

(Mahajan et al., 1994), Stenotrophomonas maltophilia CSV89

(Phale et al., 1995) and P. putida KT2442. Cultures were

grown in 150 mL mineral salt medium [MSM; Basu et al.,

2003] at 30 1C on a rotary shaker (200 r.p.m.). The medium

was supplemented aseptically with appropriate amounts of

aromatic compounds (0.1%), glucose (0.25%) or organic

acids (0.25%) as carbon source. Growth was monitored

spectrophotometrically at 540 nm.

Metabolism of glucose

Glucose grown mid-log phase cells (�200 mg) were har-

vested, washed twice with sterile distilled water, suspended

in 50 mL of 10 mM glucose prepared in sterile distilled water

and incubated at 30 1C for 3.5 h. The pH of the suspension

was constantly monitored and maintained at pH 7.0 with

KOH (6 M). After incubation, the cells were removed by

centrifugation. The supernatant was filtered through a

0.2 mm filter and lyophilized to a dry powder. Products

formed from glucose were resolved by TLC (one dimension)

and detected as described (Pujol & Kado, 2000).

Whole-cell oxygen uptake

Mid-log phase cells grown on the appropriate carbon source

were used. Respiration rates were measured at 30 1C using

oxygraph (Hansatech, UK) fitted with a Clark-type O2 elec-

trode as described earlier (Basu et al., 2003). Respiration rates

were corrected for endogenous O2 consumption and expressed

as nmol O2 consumed min�1 mg�1 of cells (wet weight).

Preparation of cell-free extracts and enzymeassays

Cell-free extracts were prepared as described earlier (Basu

et al., 2003). Protein was estimated using folin-phenol

ATP ATPATP

NAD(P)HNAD(P)

Glucose

Gluconate 2-Ketogluconate

2-Ketogluconate

Gluconate 2-Ketogluconate

Glucose

Glucose-6-P

6-P-Gluconate

2-Keto-3-Deoxy-6-P-Gluconate

Glyceraldehyde-3-P

2-Keto-6-P-gluconate

Gcd Gad

Kgt

Kgk

Kgr

GnkGck

Zwf

Pgd

Kdga

Gct

Pyruvate TCA Cycle

ATP

NAD(P)

Glucose

GluconateGlucose

Glucose-6-P

6-P-Gluconate

2-Keto-3-Deoxy-6-P-Gluconate

Glyceraldehyde-3-P

Gcd

Gck

Zwf

Pgd

Kdga

Gct

Pyruvate TCA Cycle

x xx

(a)

(b)

Fig. 1. Metabolic pathways involved in the

utilization of glucose by (a) pseudomonads and

(b) Pseudomonas putida CSV86. The enzymes

involved are: Gcd, Gad: glucose and gluconate

oxidase; Gct, Kgt: glucose- and 2-ketogluco-

nate-transporter; Gck, Gnk, Kgk: glucose-,

gluconate- and 2-ketogluconate-kinase; Zwf:

glucose 6-phosphate dehydrogenase; Kgr:

2-keto 6-phospho gluconate reductase; Pgd:

6-phosphogluconate dehydratase; Kdga: 2-

Keto-3-deoxy-6-phospho gluconate aldolase

Cross indicates the inability of strain to utilize

gluconate and 2-ketogluconate as carbon

source.

FEMS Microbiol Lett 259 (2006) 311–316c� 2006 Federation of European Microbiological SocietiesPublished by Blackwell Publishing Ltd. All rights reserved

312 A. Basu and P.S. Phale

reagent (Lowry et al., 1951). Glucose dehydrogenase (Mat-

sushita & Ameyama, 1982), gluconate dehydrogenase (Mat-

sushita et al., 1982) and glucose-6-phosphate dehydrogenase

(Lessmann et al., 1975) activities were monitored as de-

scribed. Enzyme activities are expressed either as nanomoles

of substrate consumed or product formed or NADH formed

or consumed per min. Specific activities are expressed as

nmoles per min per mg of protein.

[14C]Glucose uptake, binding assay

Uptake of [U-14C]glucose was studied by modifying the

method described previously (Sly et al., 1993). Cells were

grown till late-log phase, harvested, washed twice and

resuspended in MSM to an absorbance of 0.20 at 540 nm.

Cell suspension was incubated at 30 1C for 10 min in a

shaking water bath. To the prewarmed cell suspension

(10 mL), 5 nmol of [14C]glucose (BRIT, India, sp. ac.

140 mCi mmol�1) was added, and samples (100mL) were

withdrawn and rapidly filtered through 0.45mm cellulose

ester filters (Pall). The filters were immediately washed twice

with sterile MSM (1 mL), air dried and vigorously mixed in

scintillation cocktail (0.4% PPO and 0.025% POPOP in

toluene). Radioactivity was measured using a liquid scintil-

lation counter (Rackbeta LKB1209) and expressed as pmoles

[14C]glucose accumulated.

All the experiments were performed at least three times

in triplicate and the observed standard deviation was less

than 5%.

Results and discussion

Pseudomonas putida CSV86 metabolizes naphthalene via the

catechol meta-cleavage pathway, and benzyl alcohol via the

catechol ortho-cleavage pathway (Mahajan et al., 1994;

Basu et al., 2003). It also utilizes benzoic acid, and p-and

o-hydroxy benzoic acid and p-and o-hydroxybenzyl alcohols

(Basu et al., 2003). Besides aromatic compounds, strain

CSV86 also utilizes glucose and glycerol, but it failed to

grow on gluconate, 2-ketogluconate, fructose and mannitol.

The growth profile on various carbon sources is shown in

Fig 2. The observed specific growth rate (m, h�1) and

doubling time (h) on various carbon sources were found to

be: naphthalene (0.51, 1.36), salicylate (0.34, 2.04), benzyl

alcohol (0.54, 1.28), benzoate (0.59, 1.17) glucose (0.22,

3.15) and succinate (0.76, 0.91). Growth profile and kinetic

analysis clearly demonstrated that CSV86 utilized aromatic

compounds and organic acids faster than glucose. The

observed m and doubling time values on glucose for strains

S. maltophilia CSV89 and P. putida KT2442 were 0.52 and

1.33; and 0.55 and 1.26, respectively, indicating that strain

CSV86 utilizes glucose at a lower rate.

To elucidate the glucose metabolic pathway, O2 uptake

and enzyme activity studies were carried out. Strain CSV86

grown on glucose showed O2 uptake with glucose but failed

to respire on gluconate and 2-ketogluconate. Naphthalene-

and succinate-grown cells showed poor O2 uptake when

incubated with glucose. Strains CSV89 and KT2442 showed

O2 uptake in the presence of glucose, gluconate and 2-

ketogluconate (Table 1). These results suggest that, unlike

the other strains, CSV86 does not have the ability to

metabolize gluconate and 2-ketogluconate. These observa-

tions were supported by measurements of enzyme activities

and analysis of the products formed during metabolism of

glucose. Specific activities for various enzymes involved in

glucose metabolism are depicted in Table 2. Cell-free ex-

tracts prepared from all three strains showed activity of Zwf.

Compared with glucose-, succinate- and naphthalene-

grown cells of CSV86 showed five- to six-fold lower activity

of Zwf, suggesting that the enzyme is inducible. Strain

CSV86 showed activity of glucose oxidase but failed to show

activity of gluconate oxidase, while strains CSV89 and

KT2442 showed activity for both enzymes. TLC analysis of

metabolites produced during metabolism of glucose by

CSV86 detected very little gluconate and no 2-ketogluco-

nate; however, strains CSV89 and KT2442 showed spots

corresponding to gluconate (Rf 0.18, light blue) and 2-

ketogluconate (Rf 0.18, dark brown), data not shown.

Therefore, TLC analysis, whole-cell respiration and enzyme

activity studies suggest that CSV86 does not metabolize

glucose via gluconate and 2-ketogluconate, thus indicating

the absence of the direct oxidative pathway. However, the

presence of Zwf activity suggests that CSV86 utilizes glucose

by the phosphorylative pathway. Based on these results, the

proposed pathway for glucose metabolism in P. putida

CSV86 is shown in Fig. 1b. In strains CSV89 and KT2442,

both the phosphorylative and direct oxidative pathways

appear to be operational for glucose metabolism (Fig. 1a).

To study glucose transport, [14C]glucose uptake by cells

grown under different conditions was monitored. Glucose-

Time (h)0 5 10 15 20 25

Log

OD

540

nm

0.01

0.1

1

10

Fig. 2. Growth profile of Pseudomonas putida CSV86 on naphthalene

(�), salicylate (,), benzyl alcohol (&), benzoate (}), glucose (n) and

succinate ( ).


313Glucose metabolism in P. putida CSV86

grown CSV86 cells showed high rates of glucose uptake (Fig.

3). Addition of sodium azide (25 mM) after 1 min, inhibited

glucose uptake, and cells preincubated for 10 min with

sodium azide (25 mM) or formaldehyde (25 mM) did not

show any uptake. These results demonstrate that glucose

uptake in CSV86 is by active transport. Cells grown on

succinic acid or naphthalene alone showed very low glucose

uptake compared with glucose-grown cells. Similar results

were observed when cells were grown on benzyl alcohol or

pyruvate (data not shown). These results suggest that

glucose transport in CSV86 is suppressed when cells are

grown on organic acids or aromatic compounds.

Metabolic studies clearly demonstrated that glucose is

metabolized in P. putida CSV86 by the phosphorylative

pathway and not by the direct oxidative pathway. It has been

shown that pseudomonads sequester glucose as gluconate

and under glucose limitation conditions gluconate is uti-

lized as the carbon source (Schleissner et al., 1997). How-

ever, this is not the case with strain CSV86 as it failed to

accumulate gluconate in the medium, and did not utilize

it as a carbon source. Although a very small amount of

gluconate was formed during glucose metabolism, the

inability to utilize it as the carbon source could be due to

either lack of gluconate transport or gluconate metabolizing

enzymes, or both. CSV86 utilizes glucose at slower rate

compared with aromatic compounds and organic acids. The

slow utilization of glucose may be due to regulation of

glucose metabolizing enzymes and/or the transport process.

In strain CSV86 the activity of Zwf was found to be

inducible; five- to six-fold higher activity was observed when

cells were grown on glucose compared with naphthalene and

Table 1. Oxygen uptake rates with various substrates for Pseudomonas putida CSV86, Stenotrophomonas maltophilia CSV89 and P. putida KT2442

Substrate

O2 uptake rates (nmol min�1 mg�1)�

Pp CSV86w Sm CSV89z Pp KT2442‰

Glcz Naph Suc Glc Glc

Glucose 2.31 0.4 0.3 4.93 4.12

Gluconate ND NDk ND 0.78 4.61

2-Ketogluconate ND ND ND 0.37 1.0

�Oxygen uptake has been corrected for endogenous cell respiration.wP. putida CSV86.zS. maltophilia CSV89.‰P. putida KT2442.zCells were grown on: Naph, Naphthalene; Glc, Glucose; Suc, Succinate.kND, not detected by this method.

Table 2. Specific activities of glucose metabolizing enzymes in Pseudomonas putida CSV86 grown on naphthalene (0.1%) and glucose (0.25%), and

Stenotrophomonas maltophilia CSV89 and P. putida KT2442 grown on glucose (0.25%)

Enzyme

Specific activity (nmol min�1 mg�1 protein)

Pp CSV86

Sm CSV89 Pp KT2442Naph Glc Suc

Glucose oxidase 13 15.7 14 17.1 16

Gluconate oxidase ND ND ND 285.9 25

Glucose-6-phosphate dehydrogenase (Zwf) 14 63.4 11 95.1 170

ND, not detected.

Time (min)0 5 10 15 20 25 30 35

[14C

]Glu

cose

upt

ake

(pm

ol)

0

10

20

30

Fig. 3. [14C]Glucose uptake by Pseudomonas putida CSV86 cells grown

on naphthalene (�), succinate (,) and glucose (&). Inhibition of

[14C]glucose uptake was observed when cells were exposed to sodium

azide (25 mM) after one min (arrow,B) or pretreated for 10 min with

sodium azide (25 mM, ) or formaldehyde (25 mM, %).



succinate. The Zwf activity was 35% and 65% lower in

CSV86 compared with strains CSV89 and KT2442, respec-

tively. As reported for other pseudomonads (Midgley &

Dawes, 1973), glucose transport in CSV86 was sensitive to

sodium azide and formaldehyde demonstrating the active

transport of glucose, while significantly reduced glucose

uptake by cells grown on aromatic compounds and organic

acid indicates that this transport system is also inducible.

Based on these results, we conclude that in P. putida CSV86

the metabolism of glucose is regulated at least at enzyme and

transport level. The absence of the direct oxidative pathway

and the low activity of Zwf in CSV86 may be responsible for

the slow growth rate on glucose. Few strains have been

previously reported to have only the phosphorylative path-

way or to be defective in glucose metabolism (Lessie &

Phibbs, 1984).

It has been reported that glucose and organic acid repress

the utilization of various aromatic compounds by pseudo-

monads (Holtel et al., 1994; Schleissner et al., 1994; Muller

et al., 1996; Rentz et al., 2004) and attempts have been made

to improve the utilization of aromatic compounds in the

presence of glucose by conjugal transfer of naphthalene and

salicylate degradation genes into P. putida strains generated

by mutagenesis which are deficient in glucose metabolism

(Samanta et al., 2001). Such strains would utilize aromatic

compounds with a higher specific growth rate compared

with glucose and hence would be an asset for bioremedia-

tion. However, the viability of such strains in the environ-

ment is not known. Pseudomonas putida CSV86 is a natural

isolate and grows on aromatic compounds with a higher

specific growth rate than on glucose. It also showed a

preference for aromatic compounds over glucose and come-

tabolizes aromatic compounds and organic acids (Basu

et al., 2006). These unique properties, coupled with further

characterization and subtle modification, may make this

strain a potential candidate for bioremediation and envir-

onmental clean up.

Acknowledgements

A. B. thanks the University Grants Commission, India for

the award of a senior research fellowship.

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