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Appl Environ Microbiol. Nov 2002; 68(11): 5704–5710.
PMCID: PMC129874

Characterization of Serracin P, a Phage-Tail-Like Bacteriocin, and Its Activity against Erwinia amylovora, the Fire Blight Pathogen


Serratia plymithicum J7 culture supernatant displayed activity against many pathogenic strains of Erwinia amylovora, the causal agent of the most serious bacterial disease of apple and pear trees, fire blight, and against Klebsiella pneumoniae, Serratia liquefaciens, Serratia marcescens, and Pseudomonas fluorescens. This activity increased significantly upon induction with mitomycin C. A phage-tail-like bacteriocin, named serracin P, was purified from an induced culture supernatant of S. plymithicum J7. It was found to be the only compound involved in the antibacterial activity against sensitive strains. The N-terminal amino acid sequence analysis of the two major subunits (23 and 43 kDa) of serracin P revealed high homology with the Fels-2 prophage of Salmonella enterica, the coliphages P2 and 168, the [var phi]CTX prophage of Pseudomonas aeruginosa, and a prophage of Yersinia pestis. This strongly suggests a common ancestry for serracin P and these bacteriophages.

Bacteriocins are bacterial products with specific bactericidal activity, generally towards bacterial strains and species closely related to the producer strain (8). Two groups of bacteriocins have been described (4, 7): high-molecular-weight (HMW) bacteriocins and low-molecular-weight bacteriocins. HMW bacteriocins are thermolabile, trypsin resistant, and sedimentable by ultracentrifugation and can be induced by physical or chemical agents, which activate the SOS system (11). HMW bacteriocins have been identified in many enterobacteria (6, 13, 32, 37), Pseudomonas spp. (29), Rhizobium lupini (24), Bacillus spp. (5, 17), and Flavobacterium spp. (18).

Similarities between HMW bacteriocins and bacteriophages have been established on the basis of morphology, antigenic cross-reactivity, complementation, and DNA hybridization. Electron microscopy has revealed that HMW bacteriocins have a structure resembling that of many bacteriophage tails. Pyocin R, for example, has a contractile sheath resembling the T-even coliphage tail (29). Pyocin F has sheathless, flexible rod-like structures resembling the lambda phage tail (29).

Bacteriocins can be used in biological control, taking advantage of their specific bactericidal properties against sensitive strains. Agrocin 84, a bacteriocin produced by Agrobacterium radiobacter, is responsible for the preventive biological control of crown gall (21). Erwinia herbicola strains produce an antibiotic which may be used in the biological control of fire blight (16, 42, 44, 45). Fire blight is a typical necrotic disease which affects all plants of the family Pomoideae but is especially destructive to apple and pear trees, and it is a major problem in pip fruit production worldwide (41). Fire blight attacks all aboveground organs of the host plants, often leading to their death (36). The losses caused by this disease are considerable in Europe and the United States. In the 1970s, the losses for pears in California amounted to US$5 million (41). In 1991, the losses in southwest Michigan came to about US$4 million (28).

In addition to its geographical progression, the disease attacks new plant species (36). Prophylactic control with streptomycin has been associated with the emergence of streptomycin resistance in Erwinia amylovora. In addition, this antibiotic cannot be used in many countries because of its use in human and animal medicine (36).

In a previous work (19), we reported that Serratia plymithicum J7 produces a bacteriocin and that its induced supernatant shows activity against fire blight in vivo in greenhouse and field experiments. The aim of this work was to demonstrate that the bacteriocin produced by Serratia plymithicum J7 is involved in the activity against Erwinia amylovora, the fire blight pathogen. We purified and characterized this bacteriocin and report its similarities with some bacteriophages.


Activity spectrum of induced culture.

Serratia plymithicum J7 (CWBI collection) was grown overnight at 30°C in 60 ml of 863 medium (10 g of Bacto Peptone, 10 g of yeast extract, and 10 g of glucose per liter). The culture was harvested during exponential growth (A450 = 0.7) and divided in two. One half was treated with mitomycin C (1 mg/liter) (Sigma, Deisenhofen, Germany). After overnight incubation at 30°C, both the induced and noninduced cultures were centrifuged at 7,000 × g (20 min, 4°C); the resulting supernatants were filtered through a 0.45-μm filter (Millipore Corp., Bedford, Mass.) and stored at 4°C. Then 200 μl of each exponentially growing indicator strain (A450 = 0.7) was added to 10 ml of 863 soft agar (10 g of Bacto Peptone, 10 g of yeast extract, 10 g of glucose, and 7.5 g of agar per liter) at 55°C, mixed, and plated in petri dishes. Then 10 μl of induced Serratia plymithicum culture supernatant was spotted onto the lawn of each indicator strain. After overnight incubation at 30°C, a clear zone was taken as indicative of bacteriocin activity.

Bacteriocin assay.

Bacteriocin activity was estimated by spotting 10 μl of serially diluted sample on a lawn of the indicator strain (Erwinia amylovora B87). One activity unit (AU) is defined as the reciprocal of the last serial dilution showing a visible clear zone on the lawn prepared as described above.

Purification of serracin P.

Serratia plymithicum was grown in 11 liters of 863 medium in a 20-liter Biolafitte fermenter (Biolafitte, St. Germain-en-Laye, France). Then 500 ml of an overnight culture was used as the inoculum. Agitation, pH, aeration, and temperature were maintained at 300 rpm, 7, 0.5 vol/vol/min, and 30°C, respectively. Mitomycin C (0.7 mg/liter) was added after 3 h of growth to induce bacteriocin production.

After overnight incubation, the induced culture was centrifuged at 7,000 × g (20 min at 4°C), and the supernatant was subjected to ultrafiltration through a 10,000-Da filter (Millipore Corp., Bedford, Mass.). The retentate (0.7 liter) was centrifuged at 7,000 × g (20 min, 4°C) and filtered through a 0.45-μm filter (Millipore). This retentate was then fractionated on a Mono Q HR 5/5 column (Amersham Pharmacia Biotech) with a fast protein liquid chromatography system (Pharmacia). Proteins were eluted with a gradient of NaCl (0 to 1 M) in 20 mM Tris-HCl buffer (pH 7.7). All fractions absorbing at 280 nm were tested for bacteriocin activity against sensitive strains and retained for transmission electron microscopy analysis.

The HMW bacteriocin-containing fractions (12.5 ml, 7 mg) were pooled and concentrated by ultracentrifugation at 170,000 × g for 60 min at 4°C. The pellet was resuspended in 1 ml of elution buffer (20 mM Tris-HCl, 150 mM NaCl, pH 7.7), filtered through a 0.45-μm filter, and applied to a Sephacryl S1000 superfine column (1.6 by 60 cm) (Pharmacia) at an elution rate of 0.7 ml/min. Phages T4 (Mr, 2 × 108), lambda (Mr, 6 × 107), and MS2 (Mr, 1.8 × 106) were used as molecular weight markers. Each collected fraction (3.5 ml) was tested for bacteriocin activity against sensitive strains and analyzed by transmission electron microscopy.

Purity of the bacteriocin.

The purity of serracin P was confirmed by isoelectrofocusing and ultracentrifugation on a sucrose gradient. For isoelectrofocusing analysis, 100 μg of purified bacteriocin was electrofocused according to Wiktorsson et al. (43) in a Rotofor apparatus (Bio-Rad Laboratories, Hercules, Calif.). For purity analysis by ultracentrifugation, 600 μg of purified serracin P was subjected to overnight ultracentrifugation on a sucrose gradient (10% to 40%) at 170,000 × g and 4°C.

Transmission electron microscopy.

A negative staining technique (5) was used for transmission electron microscopy. Formvar-coated grids were deposited on drops of filtered bacteriocin suspensions (0.45-μm filter) for 10 min at room temperature, and excess suspended fluid was removed with filter paper. The grids were then washed with distilled water and negatively stained with 2% (wt/vol) potassium phosphotungstate at pH 7. The samples were examined at 100 kV accelerating voltage with a Jeol transmission electron microscope (JEM 100 SX).

Sensitivity of bacteriocin to heat and enzyme treatment.

We treated 200 μl (0.6 μg; 3.6 × 103 AU) of purified bacteriocin in 20 mM Tris-HCl-150 mM NaCl, pH 7.7, with each of the following enzymes: papain (Merck, Darmstadt, Germany; item 107144) (0.05 mg/ml, 30 min, 25°C), lipase (Fluka, Aldrich, St. Louis, Mo.; item 62311) (0.05 mg/ml, 120 min, 37°C), pronase E (Sigma, St. Louis, Mo.; item P-6911) (0.05 mg/ml, 10 min, 37°C), trypsin (Sigma; item T-7409) (2.5 mg/ml, 60 min, 25°C), and RNase (Sigma; item R-5503) (5 mg/ml, 60 min, 37°C). Bacteriocin thermostability was investigated by heating for 10 min at 40, 50, 60, and 70°C. Residual bacteriocin activity following each treatment was determined as described above.


Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) (Excel gel, 8 to 18% SDS gradient [Pharmacia]) was carried out for 80 min at 10°C in a Multiphor II apparatus (Pharmacia) at 50 mA and 600 V as described by Laemmli (23). Protein subunits were dissociated by resuspending 5 μg of lyophilized sample in 20 μl of 50 mM Tris-HCl buffer (pH 7.5) containing 0.01 g of SDS, 1.54 mg of dithiothreitol, and 0.1 mg of bromophenol blue per ml. After 5 min of incubation at 95°C, proteins bands were revealed by silver staining (Pharmacia). A low-molecular-weight calibration kit (Pharmacia) was used as a reference.

Gel electrophoresis and blotting.

SDS-PAGE was performed on an 8% gel (200 by 200 mm) with piperazine disacrylamide as the cross-linker. The gel was run for 3.5 h at 300 V in a vertical Protean electrophoresis system (Bio-Rad). The low-molecular-weight calibration kit (Pharmacia) was used as a reference. The separated proteins were electroblotted with a Novablot system at 1 V for 1.5 h at 4°C (Pharmacia), stained with Coomassie blue for 5 min, and then destained for 20 min.

N-terminal sequence analysis.

N-terminal sequence analysis of the electroblotted proteins was performed with a model 476 A pulsed liquid-phase sequenator with on-line phenylthiohydantoin analysis with a 120 A analyzer (Perkin Elmer, Applied Biosystems division). Sequencing reagents and solvents were obtained from the same company.

Amino acid composition analysis.

Gas phase acid hydrolysis of the electroblotted proteins was carried out in borosilicate glass tubes (5 by 55 mm) placed in a hydrolysis vial. We used 6 N HCl as the hydrolysis agent for 1 h at 165°C. Hydrolysis was followed by amino acid analysis on a 420 A derivatizer with on-line phenylthiocarbamyl analysis via a 130 separation system (Perkin Elmer, Applied Biosystems division).

Nucleotide sequence accession number.

The N-terminal sequence has been deposited in the Swiss-Prot database under accession numbers P83378 and P83375 for the 23-kDa and 43-kDa subunits of serracin P, respectively.


Activity spectrum of induced culture supernatant.

Induced S. plymithicum J7 culture supernatant was tested against various strains. Among the 33 strains tested, 6 showed growth sensitivity to the induced S. plymithicum J7 culture supernatant. As shown in Table Table1,1, the sensitive strains were Erwinia amylovora (the fire blight pathogen), Klebsiella pneumoniae, Serratia liquefaciens, Serratia marcescens, and Pseudomonas fluorescens.

Antibacterial spectrum of an induced S. plymithicum culture supernatant

The fire blight pathogen, Erwinia amylovora, was highly sensitive to the induced S. plymithicum J7 culture supernatant. Table Table22 shows that, in spite of their different countries of origin and host plants, all pathogenic Erwinia amylovora strains tested were sensitive to the induced S. plymithicum J7 culture supernatant. Moreover, the antibacterial activity of the S. plymithicum J7 supernatant against all sensitive strains of Erwinia amylovora increased about 100-fold upon mitomycin C induction.

Erwinia amylovora (the fire blight pathogen) strains sensitive to S. plymithicum J7 culture supernatant

Purification of S. plymithicum J7 bacteriocin.

Following cultivation and induction by mitomycin C, the bacteriocin was purified from S. plymithicum J7 cultures by ultrafiltration, ion exchange (Mono Q), and gel filtration (Sephacryl S1000) (Fig. (Fig.1).1). S. plymithicum J7 bacteriocin was purified 48.5-fold, with a final overall yield of 20.8% (Table (Table33).

FIG. 1.
Elution profile of serracin P from gel filtration on superfine Sephacryl S1000. The elution profile of concentrated bacteriocin from ion exchange chromatography (total activity, 1.9 × 107 AU) was measured at an optical density of 280 nm (thin ...
Purification of serracin P

Isoelectrofocusing and ultracentrifugation on a sucrose gradient confirmed the purity of the S. plymithicum J7 bacteriocin. These techniques demonstrated the presence of only one peak containing antibacterial activity against Erwinia amylovora B87 and identified it as an HMW bacteriocin by transmission electron microscopy analysis (data not shown).

The bacteriocin, named serracin P, displayed an isoelectric point of 5.8 and a molecular weight of approximately 7.8 × 107.

The antibacterial activity of the purified serracin P was confirmed against all sensitive strains of Erwinia amylovora mentioned in Table Table22 and against other sensitive strains mentioned in Table Table11.

Transmission electron microscopy.

Transmission electron microscopy allowed visualization of serracin P particles (Fig. (Fig.2).2). They resembled bacteriophage tail components. Complete and contracted forms of serracin P as well as empty sheaths were identified on the micrographs. The complete form was 133 nm long and 16 nm wide, and the contracted sheath was 50 nm long and 20 nm wide.

FIG. 2.
Transmission electron microscopy micrographs of serracin P produced by S. plymithicum J7. The serracin particles were visualized by negative staining with 2% potassium phosphotungstate at pH 7. (A) Induced supernatant of S. plymithicum J7. (B) Purified ...

Sensitivity of serracin P to heat and enzyme treatment.

The sensitivity of purified serracin P to enzyme hydrolysis and heat treatment was also analyzed. We found that serracin P activity was destroyed by heating for 10 min at 50°C and by pronase E treatment. In contrast, papain, trypsin, lipase, and RNase had no effect on the antibacterial activity of serracin P.


Analysis of serracin P by SDS-PAGE and silver staining showed two major bands of 23 kDa and 43 kDa and several minor bands (Fig. (Fig.33).

FIG. 3.
SDS-PAGE analysis. Protein subunits of serracin P were dissociated as described in Materials and Methods. Proteins were revealed by silver staining. Lane 1, subunits of serracin P; lane 2, molecular mass standards (low-molecular-weight calibration kit; ...

Amino acid and N-terminal sequence analysis of serracin P major subunits.

The N-terminal sequences of the 23-kDa and 43-kDa subunits were ALPKKLKYLNLFNDGFNYMGVV and DYHHGVRVL, respectively.

Homology searches of the National Center for Biotechnology Information Blast databank revealed striking homology in N-terminal sequence between the 23-kDa subunit and the coliphage 186 tube protein (77% identity), the Salmonella enterica prophage (Fels-2) (71% identity), the Pseudomonas aeruginosa prophage ([var phi]CTX) (67% identity), and the coliphage P2 tube protein (48% identity). The N-terminal sequence of the 43-kDa subunit revealed homology with the N-terminal sequences of the prophage Fels-2 (100% identity), the P2 major tail sheath protein (89% identity), the putative major tail sheath protein of Yersinia pestis prophage (89% identity), and the prophage [var phi]CTX (78% identity) (Fig. (Fig.44).

FIG. 4.
N-terminal amino acid sequence of the 23-kDa and 43-kDa serracin P subunits. (A) N-terminal sequence alignment of the 23-kDa serracin P subunit, the phage 186 tube protein (46), the Fels-2 prophage of Salmonella enterica (25), the [var phi]CTX prophage ...

For amino acid composition (data not shown), the 23-kDa subunit was found to be rich in aspartic acid (plus asparagine), glycine, lysine, leucine, serine, and arginine. The 43-kDa subunit was found to be rich in lysine, arginine, aspartic acid (plus asparagine), and leucine.


The present work shows that Serratia plymithicum J7 produces a phage-tail-like bacteriocin, known as serracin P, which is active against many strains of Erwinia amylovora, the fire blight pathogen. Furthermore, ultrastructural observations, SDS-PAGE, and N-terminal amino acid sequence analysis of its two major subunits showed similarities with several bacteriophage tails.

As reported for many high-molecular-weight bacteriocins (2, 6, 12, 37), serracin P was active against bacterial species closely related to the producer strain, yet it also appeared to inhibit Pseudomonas fluorescens 45. It is worth pointing out that in vitro, serracin P can inhibit strains important in veterinary medicine (Serratia marcescens 230, Serratia marcescens 170), in human medicine (Klebsiella pneumoniae), and above all in plant pathology (Erwinia amylovora). Indeed, serracin P showed antibacterial activity against 24 pathogenic strains of E. amylovora from different countries. Control of this pathogenic bacterium is of extreme importance in agriculture.

Many microorganisms have already been isolated as potential antagonists against E. amylovora, e.g., Erwinia herbicola, which produces antibiotics (16, 42, 44, 45), Burkholderia glumae (formerly Pseudomonas glumae), which produces tripeptide, and many other bacterial strains for which effective agents have not been determined yet (27).

We have previously reported that S. plymithicum J7 crude supernatant shows antibacterial activity against fire blight in vivo in greenhouse and field experiments (19). The efficiency of the bacteriocin was generally comparable to that of streptomycin, an antibiotic used in human and animal medicine and therefore not used for plant protection in many countries (36). In this work, we demonstrated, by purification, that serracin P is responsible for the antibacterial activity of S. plymithicum J7 supernatant against Erwinia amylovora and other sensitive strains. We showed for the first time that a phage-tail-like bacteriocin (serracin P) has the potential to be used as a means of biological control against fire blight. Prospective studies of bacteriocin formulations could certainly increase the bacteriocin efficiency, and this could be of significant importance to biological control in place of streptomycin treatment.

Ultrastructural observations and biochemical characterization of serracin P purified by anion exchange chromatography and gel filtration showed that it shared many features with other HMW bacteriocins as well as phage tail proteins.

As shown for other HMW bacteriocins (2, 37), serracin P was thermolabile and trypsin resistant. Its isoelectric point was 5.8 and its molecular weight was 7.8 × 107, i.e., higher than the molecular weights reported for marcescin A (2 × 106), pyocin F1 (3.23 × 106), and pyocin R (1.2 × 107) (10, 22, 34).

Transmission electron microscopy applied to serracin P revealed structures resembling those of T-even coliphage tails. A similar structure was reported for several bacteriocins produced by other species, such as Escherichia coli 15 (26), Pseudomonas aeruginosa (29), Proteus vulgaris (6), Rhizobacterium lupini (24), Erwinia chrysanthemi (9), Erwinia carotovora (30), Proteus mirabilis (33), Citrobacter freundii, and Flavobacterium sp. (18).

Like other HMW bacteriocins (14, 33, 39), serracin P comprises two major subunits (43 and 23 kDa) that are probably the major components of the sheath and core, respectively. A mass of 43 kDa is indeed within the molecular mass range of the other major HMW bacteriocin subunits identified as major sheath proteins, e.g., 36 kDa for pyocin R (47), 43 kDa for xenorhabdicin (39), and 46 kDa for uredovoricin 20D3 (40). Likewise, a mass of 23 kDa is within the range recorded for HMW bacteriocin subunits identified as major tube proteins, e.g., 18 kDa for pyocin R (14), 20 kDa for xenorhabdicin (39), and 21 kDa for uredovoricin 20D3 (40). For the major sheath and tube components of P2, the respective molecular masses are about 46.1 and 19.6 kDa (38).

HMW bacteriocins and some phage tails are more than just morphologically similar: antibodies against pyocin F2 and bacteriophage KF1 (22) cross-react, as do antibodies against pyocin R and bacteriophage PS17 (20). Similarity between PS17 and pyocin R has been established for six genes by antigenic cross-reactivity and complementation. In addition, similarity between the sheath genes of PS17 and pyocin R has also been established by DNA hybridization (35).

For serracin P, N-terminal sequence analysis showed that the 43-kDa and 23-kDa subunits displayed homology with the N-terminal sequences of the phage tail sheath and phage tail tube, respectively. This provides further evidence that the 43-kDa subunit (389 amino acids) and the 23-kDa subunit (171 amino acids) are indeed the major components of the sheath and tube, respectively.

Moreover, coliphages P2 and 186 display further similarities. In addition to being morphologically indistinguishable, with a straight tail about 135 nm long, P2 and 186 display serological cross-reactivity (1). The amino acid sequences of the corresponding tail sheath gene products (396 amino acids each) are 86% identical. The 186 and P2 tail tube gene products (173 and 172 amino acids, respectively) are 75% identical (38).

In conclusion, we show that serracin P, a phage-tail-like bacteriocin produced by Serratia plymithicum J7, can be a good candidate for the development of a biopesticide against the fire blight pathogen Erwinia amylovora. Furthermore, the similarities observed between serracin P and bacteriophages Fels-2, [var phi]CTX, P2, and 168 suggest a common ancestry for these bacteriophages and serracin P.


A.J. thanks the Alice Seghers Foundation for its financial help and J. L. Arpigny for revision of the manuscript.


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