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Antimicrobial Agents and Chemotherapy, March 2001, p. 901-904, Vol. 45, No. 3
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.3.901-904.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Enterocin P Causes Potassium Ion Efflux from
Enterococcus faecium T136 Cells
Carmen
Herranz,1,*
Luis M.
Cintas,1
Pablo E.
Hernández,1
Gert N.
Moll,2 and
Arnold J. M.
Driessen2
Departamento de Nutrición y Bromatología III,
Facultad de Veterinaria, Universidad Complutense, 28040 Madrid,
Spain,1 and Department of Microbiology,
Groningen Biomolecular Sciences and Biotechnology Institute,
University of Groningen, Kerklaan 30, 9751 NN Haren, The
Netherlands2
Received 24 April 2000/Returned for modification 15 August
2000/Accepted 21 December 2000
 |
ABSTRACT |
Enterocin P is a bacteriocin produced by Enterococcus
faecium P13. We studied the mechanism of its bactericidal action
using enterocin-P-sensitive E. faecium T136 cells. The
bacteriocin is incapable of dissipating the transmembrane pH gradient.
On the other hand, depending on the buffer used, enterocin P dissipates the transmembrane potential. Enterocin P efficiently elicits efflux of
potassium ions, but not of intracellularly accumulated anions like
phosphate and glutamate. Taken together, these data demonstrate that
enterocin P forms specific, potassium ion-conducting pores in the
cytoplasmic membrane of target cells.
 |
INTRODUCTION |
Antimicrobial peptides occur in a
wide range of organisms, including bacteria, plants, and animals
(10, 21). Many lactic acid bacteria produce a special kind
of antimicrobial peptides or protein, the so-called bacteriocins
(9, 20). Bacteriocins are peptides or proteins that kill
bacteria related to the producer strain. In the struggle for a niche
and nutrients, bacteriocins are useful to their producers by killing
competing bacteria. Bacteriocins have been classified into three groups
(19, 20): (i) lantibiotics, which contain
posttranslationally modified amino acids, such as lanthionine and
-methyl-lanthionine, (ii) small (<10 kDa), heat-stable peptides
without posttranslationally modified amino acids, which are subdivided
into four subgroups (IIa, peptides with the N-terminal consensus
sequence YGNGVXC, strongly active against
Listeria spp.; IIb, two-peptide systems; IIc,
sec-dependent bacteriocins; IId, class II bacteriocins not
included in the previous groups), and (iii) large (>30 kDa),
heat-labile proteins. Enterocin P is a bacteriocin composed of 44 amino
acids produced by Enterococcus faecium P13 (5)
and other related strains (11). Since it is
synthesized with a cleavable signal sequence, it may be secreted via the sec system (for a review, see reference
7). Among the sec-dependent bacteriocins
(14, 15, 24, 25), enterocin P is unique in having
both the consensus sequence YGNGVXC and a wide inhibitory
spectrum. Enterocin P is bactericidal against food-borne gram-positive
pathogenic bacteria, including Staphylococcus aureus,
Clostridium perfringens, Clostridium botulinum,
and Listeria monocytogenes (5). Here, we
studied the mode of bactericidal activity exerted by enterocin P on
enterocin-P-sensitive E. faecium T136 cells.
 |
MATERIALS AND METHODS |
Materials.
86Rb+ (10 mCi/mg),
[14C]glutamic acid (260 mCi/mmol), and
33Pi (3,000 Ci/mmol) were obtained from
Amersham, Little Chalfont, United Kingdom. Dioleoylphosphatidylcholine
(DOPC) and dioleoylphosphatidylglycerol (DOPG) were obtained from
Avanti Polar Lipids. Nisin was a gift from Aplin & Barrett. The
fluorescent probes 3-benzenedicarboxylic acid,
4,4'-[1,4,10,13-tetraoxa - 7,16 - diazacyclooctadecane - 7,16 - diylbis(5 - methosy - 6,2 - benzofurandliyl)]
(PBFI), 3,3'-dipropylthiadicarbocyanine iodide [DiSC3
(5)], and 2',7'-bis-(2-carboxyethyl)-5(and 6)-carboxyfluorescein (BCECF) were obtained from Molecular Probes, Eugene, Oreg.
Strains and culture conditions.
Enterocin P-sensitive
(T136s) (5) and enterocin P-resistant (T136r) strains of
E. faecium T136 were used in addition to the producer strain
E. faecium P13. T136r cells were isolated after selection by
treating 108 CFU of T136s cells/ml with 10,000 bacteriocin
units (BU)/ml of enterocin P for 24 h. E. faecium T136r
was not at all inhibited by an enterocin P sample that showed activity
of 7,500 BU/ml against E. faecium T136s. The enterocin P
resistance of E. faecium T136r remained stable after
culturing in the absence of enterocin P. Both enterocin P-resistant
(T136r) and enterocin P-sensitive (T136s) E. faecium T136
cells produce the enterocins A and B (4). Cells were grown
in MRS broth (Oxoid) at 30°C and harvested in the logarithmic growth phase.
Enterocin P purification and antimicrobial activity assays.
Enterocin P was purified as described previously (5). The
bacteriocin was dissolved in 60% (vol/vol) isopropanol and 0.1% (vol/vol) trifluoroacetic acid and stored at
20°C. An equal volume of the solvent without bacteriocin was used in control experiments. Bacteriocin activity was measured using a microtiter plate assay system
(12). In brief, the optical density at 660 nm of microwell cultures exposed to a range of bacteriocin concentrations was measured.
Proton motive force measurements.
The transmembrane pH
gradient (
pH) was measured by monitoring the fluorescence of the
pH-sensitive fluorescent probe BCECF (excitation wavelength, 502 nm,
and slid width, 5 nm; emission wavelength, 525 nm, and slid width, 15 nm) (17). Cells were loaded with BCECF by incubating 20 µl of 50 mM KPi cell suspension with 1 to 3 µl of 10 mM
BCECF and 2 to 2.5 µl of 0.5 N HCl for 5 min. The loading was
followed by four rapid washes (Eppendorf centrifuge, 2 min at 6,000 rpm). The transmembrane electrical potential (
) was recorded by
measuring the fluorescence of 0.5 µM DiSC3 (5)
(excitation wavelength, 643 nm, and slit width, 10 nm; emission
wavelength, 666 nm, and slit width, 10 nm) (22).
Uptake and efflux measurements.
E. faecium cells
were harvested in the logarithmic growth phase, washed, and suspended
at 137.5 µg of protein/ml in the buffers (1 to 2 ml) described in the
figure legends. Uptake of radiolabeled compounds was monitored after
the energization of the cells with 0.5% (wt/vol) glucose. After 20 min, either enterocin P (60 BU/ml) or solvent was added. At intervals,
samples (100 µl) were applied to 45-µm-pore-size cellulose nitrate
filters (Millipore Corp.) and washed twice with 2 ml of 50 mM
morpholineethanesulfonic acid (MES)-NaOH (pH 7.0) (Pi
efflux) or 100 mM LiCl. The radioactivity retained by the filters was
measured by liquid scintillation counting in a Tri-Carb 460 CD counter
(Packard Instruments Corp.).
Liposomes composed of DOPG-DOPC (1:1 [wt/wt]) and prepared by
reverse-phase evaporation (23) were loaded with
86Rb+ by overnight incubation at room
temperature. Enterocin P (80 BU/ml) or solvent was added and efflux was
measured as described above, except that filters were washed twice with
2 ml of 50 mM NaPi, pH 7.0.
K+ flux measurements.
Flux of K+ was
monitored by the K+-specific fluorescent indicator PBFI
(excitation wavelength, 336 nm, and slit width, 15.0 nm; emission
wavelength, 507 nm, and slit width, 8.0 nm) (13). Liposomes composed of DOPG-DOPC (1:1 [wt/wt]) were prepared by ethanol injection (1). Extraliposomal potassium was
removed by centrifuging potassium-loaded liposomes for 15 min at
280,000 × g.
Miscellaneous methods.
Protein concentration was measured by
the DC Protein Assay (Bio-Rad, Hercules, Calif.). The hydrophobicity
profile of enterocin P was calculated with a 19-residue window by using
the hydrophobicity scale of Eisenberg (8). Experiments
were performed at 30°C and repeated at least three independent times,
and typical experiments are presented.
 |
RESULTS |
Enterocin P-mediated 
dissipation.
The ability of
enterocin P to dissipate 
was studied by two independent methods.
First, 
was induced by energizing cells with glucose, followed by
conversion of
pH into 
by the addition of the
H+/K+ exchanger nigericin. Formation of 
resulted in a decrease in DiSC3 (5) fluorescence. Enterocin
P dissipated 
of E. faecium T136s cells in 50 mM
K-HEPES (pH 7.0) (Fig. 1B) at a
concentration-dependent rate (data not shown). By contrast, enterocin
P-resistant E. faecium T136r cells (Fig. 1A) appeared to be
completely insensitive to enterocin P action. Secondly, 
was
generated by addition of the potassium ionophore valinomycin to
nonenergized cells suspended in buffers without potassium. Under these
conditions, enterocin P did not cause any 
dissipation (data not
shown).

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FIG. 1.
Enterocin P dissipates  . Shown are enterocin
P-resistant cells (T136r) (A) and enterocin P-sensitive cells (T136s)
(B). To E. faecium cells (14 µg of protein/ml) suspended
in 50 mM K-HEPES (pH 7.0), glucose (0.5%; arrows 1) and nigericin (250 nM; arrows 2) were added, resulting in a decrease in DiSC3
(5) fluorescence and thus the generation of  . Subsequently,
enterocin P (80 BU/ml; arrows 3) and nisin (6 µM; arrows 4) were
added, resulting (eventually) in the recovery of DiSC3 (5)
fluorescence and dissipation of  .
|
|
Enterocin P elicits K+ efflux from sensitive
cells.
Since enterocin P is capable of 
dissipation, it must
conduct ion or proton movements across the membrane. Therefore, we investigated the ability of enterocin P to elicit transmembrane ion
movements. In previous experiments (C. Herranz, unpublished data), the
bacteriocin did not dissipate the
pH in energized cells, indicating
an absence of proton conductance. To exclude that ATP-consuming proton
extrusion compensated for the proton influx in these experiments,
unenergized cells loaded with the pH indicator BCECF were suspended in
50 mM KPi buffer, pH 6.5. Addition of enterocin P did not
affect the BCECF fluorescence. In contrast, nigericin drastically
reduced the BCECF fluorescence (data not shown). These data confirm
that enterocin P does not conduct proton movements.
Subsequently, the effect of enterocin P on transport of the potassium
ion analog
86Rb
+ was evaluated.
Glucose-energized cells rapidly accumulated
86Rb
+ (Fig.
2). Addition of
enterocin P to
E. faecium T136s cells resulted
in rapid
(time required to deplete the intracellular concentration
of
radioactive substrate to 50% [
t50], <3 min)
and drastic (more
than 98%) efflux of
86Rb
+.
In contrast, enterocin P did not cause any
86Rb
+ efflux from either the producer
(
E. faecium P13) (data not shown)
or the
enterocin P-resistant (
E. faecium T136r) strain (Fig.
2)
or large unilamellar PC-PG liposomes (data not shown). In all
experiments that are represented in Fig.
2, addition of enterocin
P
caused the complete efflux of rubidium ions within 10 min, whereas
the
rubidium content of the resistant and producer cells did not
decrease
at all. In order to verify the potassium ion efflux,
experiments were
performed with the potassium ion-specific fluorescent
probe PBFI.
Addition of glucose to a cell suspension with external
PBFI
resulted in a decrease in the fluorescence due to potassium
uptake
(Fig.
3). Subsequent addition of
enterocin P caused a reversal
of the PBFI fluorescence, indicating
the release of potassium
ions. Synthetic PC-PG liposomes, loaded
with PBFI and KP
i buffer
or just with KP
i, were
insensitive to enterocin P treatment at
the concentrations tested (data
not shown).

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|
FIG. 2.
Enterocin P causes the efflux of
86Rb+ from sensitive cells. Cells (137.5 µg
of protein/ml) suspended in 50 mM NaPi were energized with
0.5% glucose, thus allowing 86Rb+ uptake. At
the arrow, enterocin P (60 BU/ml) was added to E. faecium
T136s ( ), E. faecium P13 ( ), and E. faecium
T136r ( ) cells and solvent was added to E. faecium T136s
( ) cells.
|
|

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|
FIG. 3.
Enterocin P conducts potassium ion movements in
sensitive cells. E. faecium T136s cells (14 µg of
protein/ml) were energized (0.5% glucose; arrow 1), after which
solvent (arrow 2) or enterocin P (60 BU/ml; arrow 3) and valinomycin
(0.25 µM; arrows 4) were added.
|
|
Enterocin P does not induce anion efflux.
E.
faecium T136 cells treated with 60 BU/ml of enterocin P showed
neither an inhibition of phosphate uptake nor efflux of accumulated
phosphate. Efflux was only observed after addition of nisin (data not
shown), which is known to form pores in the target membrane. A higher
concentration of enterocin P (130 BU/ml) slowed down the phosphate
uptake without causing any efflux (data not shown). The effect of
enterocin P on transport of glutamate by E. faecium T136
cells was also determined. E. faecium T136 cells rapidly
accumulated the glutamate (data not shown). A decrease in the cellular
radioactivity was observed even before enterocin P or solvent addition,
and this is likely due to rapid metabolization of the accumulated
glutamate. There was no difference in the efflux observed between the
presence of enterocin P or only solvent. On the other hand, nisin
caused a significant and rapid release of the glutamate (data not
shown). Enterocin P also did not inhibit uptake of glutamate (data not
shown). These results suggest that enterocin P does not form aspecific pores.
 |
DISCUSSION |
Here, we investigated the bactericidal action of the bacteriocin
enterocin P by studying its effect on transport processes in E. faecium T136s cells. Enterocin P causes a rapid and drastic efflux
of the intracellularly accumulated potassium ion analog 86Rb+ from E. faecium T136s cells.
Efflux of potassium ions measured by the specific fluorescent probe
PBFI shows a rapid release of intracellular K+. This
enterocin P-mediated potassium ion efflux is highly specific, as under
the same sets of conditions, no dissipation of the
pH was observed.
Moreover, the collapse of the 
occurred only under specific
conditions. No enterocin P-mediated dissipation is observed for a
valinomycin-induced 
in cells suspended in Na+ or in
choline-containing buffers. This indicates that the bacteriocin conducts neither sodium or choline ion influx. Finally, enterocin P
does not cause efflux of ATP (Herranz, unpublished), radiolabeled phosphate, or glutamate.
Enterocin P has no activity at all against the producer and resistant
cells nor does it seem to act on synthetic liposomes. A putative
immunity protein-encoding gene is present in the producer E. faecium P13 cells (5). One might speculate that a
receptor-like factor, which is absent in synthetic liposomes, might be
dysfunctional in the resistant cells. However, the bacteriocin has
activity against species from a variety of genera (5),
which reduces the likelihood of a required cell factor.
Strikingly, enterocin P resembles the two-component bacteriocin
lactococcin G in its high capacity to conduct potassium ions whereas
there is no conductance of protons. In contrast to enterocin P,
lactococcin G conducts a range of monovalent cations, including sodium
and choline ions (18). The two-component lantibiotic lacticin 3147 dissipates
pH only indirectly after prolonged
incubation that results in a depletion of the ATP pool
(16).
Various mechanisms of membrane permeabilization by antimicrobial
peptides have been proposed: the wedge-like model (6), the transmembrane helical bundle of hydrophobic peptides, the thoroidel
model, the in-plane diffusion model, and the carpet model
(3). Enterocin P pores may be composed of transmembrane bundles of hydrophobic peptides. This is supported by the high ion
specificity of enterocin P and by the presence of a highly hydrophobic
transmembrane segment in the C-terminal part of enterocin P (Fig.
4). Since the hydrophobicity increases in
the N-to-C-terminal direction, the C-terminal segment of enterocin P
may possibly insert into the membrane, whereby the C-terminal histidine
reaches the cytoplasm. In this respect, a C-terminal intracellular
histidine has been shown to determine the activity of a potassium
channel (2).
Taken together, bundles of transmembrane enterocin P peptides may form
a pore that specifically conducts potassium ions. Future reconstitution
of potassium ion-conducting enterocin P activity in liposomes may
reveal the molecular interactions that underlie the observed high ion
specificity of enterocin P pores.
 |
ACKNOWLEDGMENTS |
This work was partially supported by grants ALI-97-0559 and
AGL2000-0707 from the Comisión Interministerial de Ciencia y Tecnología (CICYT), Madrid, Spain. C. Herranz is the recipient of a grant from the Ministerio de Educación y Ciencia, Spain.
 |
FOOTNOTES |
*
Corresponding author. Mailing address: Departamento de
Nutrición y Bromatología III, Facultad de Veterinaria,
Universidad Complutense, 28040 Madrid, Spain. Phone:
34913943750. Fax: 34913943743. E-mail:
cburgy{at}eucmax.sim.ucm.es.
 |
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Antimicrobial Agents and Chemotherapy, March 2001, p. 901-904, Vol. 45, No. 3
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.3.901-904.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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