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J Bacteriol, April 1998, p. 2133-2136, Vol. 180, No. 8
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Availability of O2 as a Substrate in
the Cytoplasm of Bacteria under Aerobic and Microaerobic
Conditions
Tanja
Arras,
Jan
Schirawski, and
Gottfried
Unden*
Institut für Mikrobiologie und
Weinforschung, Universität Mainz, 55099 Mainz, Germany
Received 5 December 1997/Accepted 17 February 1998
 |
ABSTRACT |
The growth rates of Pseudomonas putida KT2442 and mt-2
on benzoate, 4-hydroxybenzoate, or 4-methylbenzoate showed an
exponential decrease with decreasing oxygen tensions (partial
O2 tension [pO2] values). The oxygen tensions
resulting in half-maximal growth rates were in the range of 7 to 8 mbar
of O2 (corresponding to 7 to 8 µM O2) (1 bar = 105 Pa) for aromatic compounds, compared to 1 to
2 mbar for nonaromatic compounds like glucose or succinate. The
decrease in the growth rates coincided with excretion of catechol or
protocatechuate, suggesting that the activity of the corresponding
oxygenases became limiting. The experiments directly establish that
under aerobic and microaerobic conditions (about 10 mbar of
O2), the diffusion of O2 into the cytoplasm
occurs at high rates sufficient for catabolic processes. This is in
agreement with calculated O2 diffusion rates. Below 10 mbar
of O2, oxygen became limiting for the oxygenases, probably
due to their high Km values, but the diffusion
of O2 into the cytoplasm presumably should be sufficiently
rapid to maintain ambient oxygen concentrations at oxygen tensions as
low as 1 mbar of O2. The consequences of this finding for
the availability of O2 as a substrate or as a regulatory
signal in the cytoplasm of bacterial cells are discussed.
| |
INTRODUCTION |
During aerobic growth, bacteria
consume O2 at high rates. The consumption of O2
by oxidases takes place on the cytoplasmic side of the membrane. Since
the diffusion of O2 across the membrane is rapid, the
supply of the oxidases with O2 is guaranteed even at the
very low O2 tensions which are sufficient for aerobic
growth (<1 mbar of O2) (2, 4, 15, 16).
Previously, the rate of O2 diffusion into the cytoplasm of
Escherichia coli was calculated from the cell dimensions and
the diffusion coefficients and compared to the rates of O2
consumption (2, 21, 22). It was estimated that at
O2 tensions as low as 0.2 mbar of O2
(corresponding to 0.2 µM O2), the supply of
O2 by diffusion exceeds the consumption by respiration. In
agreement with this calculation, in E. coli the fermentation
pathways were synthesized and used only at partial O2
tension (pO2) values well below 1 mbar of O2
(3). Thus, O2 is able to reach the active sites
of the oxidases at rates sufficient to support aerobic respiration even
at very low O2 tensions.
The O2 supply of the cytoplasmic space is not known and
might be different from that of the membrane where the oxidases are located. From the diffusional parameters and the cell dimensions, it
was calculated that the concentrations of O2 should be the same within and outside the bacteria at O2 tensions as low
as 1 mbar of O2 (21, 22). Therefore, we aimed
for an experimental proof of the availability of O2 in the
bacterial cytoplasm under aerobic and microaerobic conditions.
For the degradation of aromatic compounds like benzoate, oxygenases are
required for oxidative cleavage of the aromatic ring (7,
10). Due to the cytoplasmic location of the oxygenases and the
need for molecular oxygen as a cosubstrate, the turnover of aromatic
compounds depends on the availability of O2 in the cytoplasm. The rate of metabolism of aromatic compounds therefore provides information on the minimal rate of O2 diffusion
into the cytoplasm. To this end, the relation of metabolism of various aromatic compounds to the pO2 of the medium was studied.
Pseudomonas putida KT2442 degrades benzoate by
benzoate-1,2-dioxygenase and catechol-1,2-dioxygenase (ortho
pathway), whereas 4-hydroxybenzoate is degraded via 4-hydroxybenzoate
monooxygenase and protocatechuate-3,4-dioxygenase (ortho
cleavage). 4-Methylbenzoate is metabolized by P. putida mt-2
by toluate-1,2-dioxygenase and catechol-2,3-dioxygenase
(meta cleavage) (5, 8). The
Km values for O2 of the oxygenases (
7 µM) (1, 6, 12, 13) are much higher than those of the
oxidases (<0.1 µM) (4, 15, 16). Therefore, limitation of
growth or catabolism by O2 must be due to the oxygenases,
and information on O2 diffusion into the cytoplasm and the
O2 concentration in the cytoplasm can be drawn from the
growth-limiting pO2 values. Here we report on experimental
proof of the availability of O2 in the cytoplasm. This
finding also provides a basis for our understanding of the
O2 sensing by cytoplasmic O2 sensor proteins
like FNR (fumarate nitrate reductase regulator) from E. coli
(9, 19, 22, 23) and the homologous proteins from
Pseudomonas (17, 25) which are supposed to react
directly with O2 in the cytoplasm (2, 22, 23).
| |
MATERIALS AND METHODS |
Bacteria and media.
P. putida KT2442 and P. putida mt-2(pWWO) were provided by I. Wagner-Döbler
(Braunschweig, Germany) and M. Schlömann (Stuttgart-Hohenheim, Germany) (5, 24). P. putida KT2442 was grown in a
modified M9 mineral medium (pH adjusted to 7.1) supplemented with a
mineral salts solution and with glucose, succinate, benzoate, or
4-hydroxybenzoate (10 mM each) as sources of carbon and energy. The
mineral salts solution was a combination of the following: solution 1, containing 25.39 g of MgCl2, 2.0 g of
CaCO3, 4.5 g of FeSO4 · 7H2O, 0.85 g of MnSO4 · H2O, 1.44 g of ZnSO4 · 7H2O, 0.25 g of CuSO4 · 5H2O, 0.16 g of CaSO4 · 0.5H2O, and 0.02 g of H3BO3
dissolved in 51.3 ml of concentrated HCl and with water added to 100 ml; solution 2, containing 360 mM FeSO4 · 7H2O; and solution 3, containing 1 M MgSO4.
Solutions 1 and 2 were filter sterilized, and solution 3 was
autoclaved. Then 50 ml of solution 1, 2.5 ml of solution 2, 25 ml of
solution 3, and 22.5 ml of autoclaved H2O were combined. The medium was supplemented with 0.25 ml of the resulting mineral salts
solution per 100 ml. P. putida mt-2(pWWO) was grown in a phosphate-buffered medium (14.0 g of
Na2HPO4 · 12H2O, 2.0 g
of KH2PO4 per liter) supplemented with a salts
solution (20 ml/liter of medium) containing 2.5 g of
Ca(NO3) · 4H2O (autoclaved separately) per liter, 0.5 g of Fe(III)NH4-citrate per liter,
10 g of MgSO4 · 7H2O per liter,
50 g of (NH4)2SO4 per liter,
and 50 ml of the Pfennig SL6 metal salts solution (14) per
liter. The C source for P. putida mt-2 was 4-methylbenzoate
(10 mM). E. coli MC4100 (18) was grown in M9
medium (11) supplemented with an amino acid mixture
(20) and glucose (10 mM) or succinate (10 mM).
Growth.
P. putida was grown at 30°C. Growth under
anaerobic conditions was performed in sealed bottles under an
atmosphere of nitrogen (2, 3). For aerobic conditions, the
bacteria were grown in Erlenmeyer flasks filled to within 10% of the
maximal volume under vigorous shaking (3). The medium was
inoculated from cultures grown overnight under aerobic conditions in
the mineral medium (same C source as that in the main culture) to an
A578 not higher than 0.06.
Growth in an oxystat.
Growth at defined O2
tensions (pO2) was performed in an oxystat (chemostat with
constant pO2) (Biostat MD; Braun, Melsungen, Germany) in
batch culture (1.5 liters) with constant stirring (400 rpm) (2,
3). The pO2 value of the medium was measured continuously with an O2 electrode. The pO2 was
maintained at a constant level by supplying air (valve I) and
N2 (valve II) to the vessel. When the pO2 fell
below 98% of the set value, valve I opened and sterile air was
supplied till the set value was reached. The flow of air was increased
manually from about 0.16 to 1.6 liters min
1 during growth
to compensate for the increasing O2 consumption. The flow
of N2 (0.1 liters min1) was decreased or
switched off as required. E. coli was grown in the oxystat
in the supplemented M9 medium as described previously (2,
3). Growth rates were calculated from µ = ln
(A578,t2/A578,t1) · (t2 
t1)1, where
t2 and t1 are the times
of measurement and
A578,t1 and
A578,t2
are the absorbance values at 578 nm measured at
t1 and t2, respectively.
Analytical procedures.
Substrates (glucose, succinate,
benzoate, 4-hydroxybenzoate, and 4-methylbenzoate) and products
(catechol, protocatechuate) were determined from the supernatants of
the cultures after removal of the bacteria by centrifugation. The
substances were analyzed by high-performance liquid chromatography
(HPLC) on an Aminex HPX87H column (300 by 7.8 mm; Bio-Rad) with 6.5 mM
H2SO4 as the eluent (flow rate, 0.55 ml
min1) as described previously (20). The
following substrates and products were determined and quantified with
standard solutions by a refractive index and by a UV light detector
(215 nm): glucose, glycerol, acetate, ethanol, formate, pyruvate,
fumarate, succinate, and lactate. Benzoate (retention time
[Rt] = 68 min), 4-hydroxybenzoate (Rt = 51 min), catechol
(Rt = 32.0 min), and protocatechuate
(Rt = 33.3 min) were identified by the
Rt values of authentic substances, and the ratio
of the refractive index/UV absorption at 215 nm was used to confirm the
identities.
| |
RESULTS AND DISCUSSION |
Growth of P. putida on aromatic compounds at limiting
pO2.
P. putida was grown on nonaromatic and
aromatic substrates like glucose, succinate, and benzoate in an oxystat
at defined pO2 values. In the oxystat, the set
pO2 values could be maintained constant for the duration of
the growth experiment. With glucose or succinate as the substrate, the
growth behavior changed only when the pO2 fell below 10 mbar of O2 (corresponding to about 10 µM O2).
At lower pO2 values, the growth rate and final cell density
decreased, and under anaerobic conditions, no growth was observed. With
benzoate or 4-hydroxybenzoate as the substrate, under aerobic
conditions (212 mbar of O2; air saturation), growth of
P. putida (Fig. 1A) was
similar to that on glucose or succinate. However, with decreasing
pO2 values, growth rate and yield decreased significantly.
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FIG. 1.
Growth (A) and growth rates (B) of P. putida
KT2442 grown in an oxystat on aromatic and nonaromatic substrates as a
function of pO2. (A) Growth with benzoate in the oxystat at
different pO2 values. Growth was performed in the mineral
medium with 10 mM benzoate at 212 ( ), 21 ( ), 8 ( ), 6 ( ), 4 ( ), and 0 ( ) mbar of O2. (B) The rate constants for
growth (µ) were determined from the growth curves shown in panel A. Substrates (10 mM each) for growth: benzoate (), 4-hydroxybenzoate
(), glucose (), and succinate ().
|
|
In Fig.
1B, the rate constants for growth on aromatic and nonaromatic
substrates are plotted versus the pO
2 values. With glucose
and succinate, growth of
P. putida commenced at very low
pO
2 values
and showed a saturation curve with increasing
pO
2. With the aromatic
substrates benzoate and
4-hydroxybenzoate, growth started only
at pO
2 values above
4.2 mbar. With 4-methylbenzoate, the O
2 requirement
was
even higher (data not shown). The maximal growth rates for
succinate
and benzoate corresponded to doubling times of 46 and
51 min,
respectively. When
E. coli was grown on succinate or
glucose,
the growth rates increased immediately from 0 mbar, similar to
the growth rates of
P. putida on the same substrates (data
not
shown). For growth on glucose, however, the growth rates did not
drop to zero at 0 mbar of O
2 due to the presence of
fermentative
growth. Thus, the growth rate at 0 mbar of O
2
(µ = 0.011 min
1) was about half that of
E. coli grown under aerobic conditions
on glucose (µ = 0.020 min
1).
pO0.5 values for growth on aromatic substrates are
higher than those for growth on nonaromatic substrates.
For
P. putida, from the relation of the growth rates to the
pO2 values, the pO0.5 values for the substrates
can be determined. The pO0.5 value corresponds to the
pO2 value yielding half-maximal growth rates (2,
3). The measured pO0.5 values can be classified into
two groups. For growth of P. putida and E. coli
on glucose and succinate, low values (pO0.5 
2 mbar of
O2) were found. For growth on aromatic compounds, the
pO0.5 values were distinctly higher and corresponded to
about 8 mbar for growth on benzoate and 4-hydroxybenzoate and to 19 mbar for growth on 4-methylbenzoate.
Excretion of intermediates under O2 limitation.
The growth medium was analyzed for products or intermediates excreted
by the bacteria during growth in the oxystat at different pO2 values (Fig. 2). The
medium was analyzed by HPLC for the presence of organic acids,
alcohols, sugars, and aromatic compounds, in particular for
intermediates of the respective metabolic routes. During growth at high
oxygen tensions, all types of substrates were completely oxidized by
P. putida and no organic end products were detected in
significant amounts (>0.05 mol/mol of substrate). From glucose and
succinate, no end products were excreted even at decreased oxygen
tensions, indicating complete oxidation. When P. putida
KT2442, however, was grown on benzoate, a product was found in the
medium at oxygen tensions below 20 mbar which was identified as
catechol. Catechol is an intermediate of the ortho cleavage
pathway of benzoate. Up to 0.65 mol of catechol per mol of benzoate was
measured, indicating a severe limitation in the ortho
cleavage pathway resulting in the excretion of the intermediate without
complete oxidation. During growth on 4-hydroxybenzoate, protocatechuate
was excreted in large amounts (0.28 mol/mol of 4-hydroxybenzoate) at
oxygen tensions below 20 mbar. Obviously, limitation of
protocatechuate-3,4-dioxygenase activity (6) by low
O2 tensions causes accumulation and excretion of the
intermediate protocatechuate. Therefore, in both pathways, central
steps, i.e., the dioxygenases reacting on catechol and protocatechuate,
are limiting under microaerobic conditions.
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FIG. 2.
Products in the culture medium of P. putida
KT2442 excreted after growth at various pO2 values in the
oxystat: catechol () excreted during growth on benzoate (10 mM),
protocatechuate () excreted during growth on 4-hydroxybenzoate, and
end products () from succinate and glucose. For end products tested,
see Materials and Methods.
|
|
Availability of O2 as an intracellular substrate for
aromatic substrate degradation.
The data can be used to roughly
estimate the rate of O2 diffusion into the cells required
for this process. The rate of O2 consumption by the
oxygenases in the cell interior
(
O2in) is twice the rate of
benzoate metabolism (benzoate) (Table
1) corresponding to 0.22 mmol of
benzoate · min1 · g (dry
weight)1 and 0.44 mmol of O2 · min1 · g (dry weight)1. The
calculated rate of O2 diffusion into the cells under
aerobic conditions, 360 mmol of O2 · min1 · g (dry weight)1 (Table 1),
exceeds the rate of intracellular O2 consumption by the
oxygenases by 3 orders of magnitude.
Plotting the rates of growth on benzoate as a function of the
pO
2 shows that diffusion of O
2 is not limiting
under aerobic
or microaerobic conditions (Fig.
3): growth is limited apparently
only at
pO
2 values below 10 mbar of O
2. The growth
limitation
coincides with the excretion of the oxygenase substrates
catechol
and protocatechuate, demonstrating that oxygenation is the
growth-limiting
step. At 10 mbar of O
2, the calculated
diffusion is still higher
by 2 orders of magnitude than the
O
2 consumption by the oxygenases
(Fig.
3). Therefore, the
decrease in the growth rate is presumably
not caused by limiting
O
2 diffusion but by the high
Km
value (20
µM) of the oxygenase (Table
1). Thus, at pO
2
values as low as
10 mbar, there is substantial O
2 present
in the cytoplasm. The
high
Km values of the
oxygenases prevented an analysis of the
situation at lower
pO
2 values. The calculation of the diffusion
rates for
O
2, however, also suggests that at distinctly lower
oxygen
tensions, down to 1 mbar of O
2, the intracellular
pO
2 equals
the extracellular pO
2 (
2,
21,
22). The O
2 present under
aerobic and microaerobic
conditions most likely is also used as
the signal for O
2
sensor-regulator proteins like FNR from
E. coli (
9,
22) and homologous proteins from
Pseudomonas strains
(
17,
25) which are thought to react directly with
O
2 in the
cytoplasm (
2,
23). The regulatory
pO
0.5 which causes a switch
from active (anaerobic) to
inactive (aerobic) FNR is in the range
of 1 to 5 mbar of O
2
in the external medium for many target genes,
which is in good
agreement with the results found in the present
work.
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FIG. 3.
Growth rate, O2 consumption by dioxygenases,
and maximal rate of O2 diffusion into the bacteria
(P. putida KT2442) as a function of the pO2 in
the medium during growth on benzoate. The growth rate was determined as
described in the legend to Fig. 1. The O2 consumption by
the dioxygenases was calculated from µ and from the molar growth
yield on benzoate (Ybenzoate) under the
respective conditions as shown in Table 1. The rate of diffusion into
the bacteria was calculated as a function of external oxygen
concentration (with the internal concentration set at zero). For the
calculation, the diffusion coefficients of O2 in water,
phospholipid, and cytoplasm and the cell dimensions were used (2,
22).
|
|
| |
ACKNOWLEDGMENTS |
We are grateful to Deutsche Forschungsgemeinschaft and the Fonds
der Chemischen Industrie for financial support, to D. Vlad for HPLC
analysis, and to I. Wagner-Döbler (Braunschweig, Germany) and M. Schlömann (Stuttgart-Hohenheim, Germany) for supplying strains.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Institut
für Mikrobiologie und Weinforschung, Universität Mainz,
Becherweg 15, 55099 Mainz, Germany. Phone: 49-6131-393550. Fax:
49-6131-392695. E-mail: unden{at}mzdmza.zdv.uni-mainz.de.
| |
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J Bacteriol, April 1998, p. 2133-2136, Vol. 180, No. 8
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Top
Abstract
Introduction
