ABSTRACT. Two types of actinophages, 0S and 4,L, were isolated from soil samples by using Streptomyces scabies, a potato scab pathogen, as indicator strain.
Folia Microbioi. 46 (6), 519-526 (2001)
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Isolation and Characterization of Two Types of Actinophage Infecting Streptomyces scabies EL-S.A. EL-SAVED, G. EL-DIDAMONY, K. MANSOUR Department of Botany, Faculty of Science, Zagazig University,Zagazig, Egypt Received 30 July 2001 ABSTRACT. Two types of actinophages, 0S and 4,L, were isolated from soil samples by using Streptomyces scabies, a potato scab pathogen, as indicator strain. The phages were partially characterized according to their physicochemical properties, plaques and particles morphology, and their host range; this varied from narrow (for d/S) to wide (for d#L). The adsorption rate constants of the ddS and ~bL were 3.44 and 3.18 pL/min, and their burst sizes were 1.61 and 3.75 virions per mL, respectively. One-step growth indicated that 4~S and ~bL have a latent period of 1/2 h followed by a rise period of 1/2 h. The temperate character of these phages was tested in other isolates of Srreptomyces. Four of
the phages (d~SS3, d?SS12, ~bSS13and ~bSS17)were identified as temperate phages, since they were able to lysogenize SS3, SS12, SS13 and SS17. tlkSS3, ~SS12 and ~SS13 were homoimmune, and they were heteroimmune with respect to d#SS17. The restriction barriers of lysogenic isolates (SS12, SS13 and SS17) interfered with the blockage of plaque formation by phages (~SS12, ~SS13 or qbSS17) propagated on them, about 75 % of lysogenic isolates had restriction systems. The exposure of the lysogenic isolates (SS12, SS13 and SS17) to UV-irradiation prevented the possible restriction barriers of these isolates so that these barriers could be overcome.
'lhe economic importance of streptomycetes has stimulated the construction of cloning systems using both plasmids and some suitable phages as vectors (Thompson et al. i98o; Chater I986; Cresswell et al. I992). Most phages have been isolated from soil in which they are widespread, but some isolates were obtained from lysogenic wild-type strains. Viruses which infect members of the actinomycetes are called actinophages; they have played an important role as taxonomic tools for phage typing of streptomycetes (Kutzner x96i; Korn-Wendish and Schneider I992; Kurtboke 1996), and for the examination of host restriction barriers (Lomovskaya et al. i98o; Chater I986; Schneider et al. I99o; Hahn et al. 1990 ). Many Streptomyces spp. produce type II restriction endonucleases (Roberts I988). Their expression in streptomycetes can block infection by bacteriophages that contain the corresponding cleavage sites in their DNA (Chater and Wilde x98o; Cox and Raltz I984; Shirai et al. I99I). Many streptomycete phages lack cleavage sites for subsets of restriction barriers produced by streptomycetes (Anne et al. ]984; Foor et al. I985; Diaz et al. I989, I990. The strong correlation between the expression of restriction and the blockage of plaque formation for certain bacteriophages suggested that about 80 % of Streptomyces species express significant restriction barriers (Cox and Baltz I984). The broad host range of streptomycete phages, on the average, form plaques on about 50 % of the hosts tested (Cox and Baltz I984; McHenney and Baltz I989). Generally, the actinophages with the wide host range infected several genera or species of actinomycetes (Foor et al. I985; E1-Tarabily et al. I995; Kurtboke I996; Ogiso et al. 1999). On the other hand, Anne et al. (I984), Diaz et al. 0989), and Nishiwaki et al. 0996) reported that some phages have a relatively narrow host range. Study of lysogeny in actinomycetes encounters more difficulties than in other bacterial system. The occurrence of true lysogeny in members of the genus Streptomyces by any phage isolated from natural sources was shown by Welsch (I956, I959). Lysogenic cultures were found to exist when they released phages capable of forming plaques on sensitive indicator strains (Lomovskaya et al. 1972; Dowding and Hopwood I973; Chater and Carter I979; Chater and Wilde i98o; Anne et al. I984, I99O). In this study we report the isolation from soil of two phages having the ability to form plaqueg on S. scabies and their preliminary characterization; we analyzed the interaction of these phages with other isolates of Streptomyces. In addition, examinations of cross immunity of the temperate phages causing lysogenic isolates, as well as production of restriction barriers by these isolates are reported.
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MATERIALS AND METHODS
Organisms and culture conditions. Streptomyces scabies strain MR13 was provided from the Mircen Culture Collection, Faculty of Agriculture, Ain-Shams University, Ain-Shams (Egypt). The other pathogenic isolates (strains S-63 and S-64) were isolated from potato tubers with scab symptoms and produced thaxtomin A (EI-Sayed 2ooo). Nonpathogenic isolates were isolated from Egyptian soil according to Davis and Williams (~97o). The grouping and identification characteristics of the nonpathogenic isolates were studied by using articles of ISP (Shirting and Gottlieb 1966) and the key of Bergey's Manual (I989). These isolates were identified as Streptomyces sioyaensis SS1 and SS2, S. pluricolorescens SS3 and SS4, S. plicatus SS5, SS6 and SS7, S. coeruleombidus SS8, SS9 and SS10, S. albus SSll, S. nigellus SS12, S. fulvoviridis SS13, SS14, SS15, SS16, and S. spheroides SS17. Phage isolation. Phages infecting S. scabies MR13 were isolated trom irrigated soil with sewage water following essentially the enrichment method of Dowding (I973). Samples of soil extract were prepared according to Welsch et al. (x955). 0.1 mL of sterile soil extract was added to YEME broth (10 mL) containing spores (~106) of S. scabies MR13. After overnight incubation at 30 ~ with shaking, samples were centrifuged (frequency 50 Hz) and supernatants were sterilized by passage through MiUipore filters (0.45 ~m). Phages were detected by plating in soft agar overlays (Adams x959), using S. scabies MR13 as indicator strain; they were distinguished by differences in plaque morphology, size and turbidity, and were purified by serial replating from single plaques. Two actingphage isolates were studied. Propagation of actinophages. To obtain phage suspensions of high-titer lysates, confluent plate lysates were prepared according to Anne et aL (I984). On solid medium, lysates could be harvested after 20 h of cultivation. Shaking-flask lysates were prepared by adding 100 PFU/}xL to 200 mL cultures containing homogenized mycelia of the indicator strain (10 CFU/nL). Incubation was carried out at 30 ~ and 2 Hz for 40 h. Bacteria was removed by centrifugation (85 Hz, 10 rain). Phage propagation was sterilized by passage through 0.45 ~m Millipore filters. Morphological studies. Phage particles from high-titer lysates were deposited on copper grids (200 mesh) with carbon coated collodion membrane. The grids were then negatively stained with 2 % (W]V) uranyl acetate and observed under transmission electron microscopy. Host-range determination. Plaque formations by serial dilutions of each phage was used rather than qualitative spot tests to determine the host range of the phages, using S. scabies MR13, S-63 and S-64 (scab pathogens), and 17 nonpathogenic Streptomyces isolates. Spores were collected from YEME plates ( 2 - 3 weeks old) and suspended in 0.5 mL sterile water. These spore suspensions were mixed with YEME soft agar (0.8 % agar, 10 mL) and plated in Petri dishes. Within 3 h, suspension of actingphage isolates tested (20 I~L, 10 PFU/nL) was dropped on these plates. Infection could be scored by the presence of plaques in lawn of Streptomyces isolates after a 3-d incubation at 30 ~ Adsorption rate of phages. The adsorption experiment was carried out with the two isolated phage suspensions added to spores of their indicator host (S. scabies MR13). Suspension of each phage was incubated at 30 ~ with gentle shaking. Samples were withdrawn at regular intervals after contact. The mycelial fragments of the indicator strain were removed by centrifugation (5 rain, 85 Hz) and the concentration of phage remaining in the supernatant was counted. The adsorption rate of the two phages was determined by measuring residual plaque-forming ability in membrane-filtered samples of an attachment mixture (Dowding I973) and the adsorption rate constant K (mL/min) was calculated (Adams x959). A one-step with experiment was conducted as described by Dowding (x973). Determination of lysogeny. Lysogenization of the host range was demonstrated according to Schneider et al. (I99O). Broth cultures of different growth stages of each phage were filtered through a 0.45-1~m membrane filter and 50-~L volumes were spotted onto fresh lawn of possible various indicator strains. When lysed zones appeared after 1V2 d incubation at 30 ~ material of these spots was streaked over an agar plate (base layer). In order to obtain single plaques, the plates were overlaid with a top layer containing spores of the same strain as was used to detect the phage from the culture supernatant. The phages thus detected usually give rise to turbid plaques with growth of lysogenized indicator strains. Plaques with growth of indicator strains were streaked over agar plates, incubated for 189d at 30 ~ and overlaid with spores of the indicator strain. Lysogenized colonies releasing phages were therefore surrounded by lysis zones within the indicator lawn. These lysogenic bacteria were immune to superinfections by the same phage. UV treatment. The lysogenlc isolate derivatives (S. nigellus SS12, S.fulvoviridis SS13 and S. spheroides SS17) exhibited considerable restriction barriers for the temperate phages. In order to overcome these barriers high phage titres were used. In some cases, however, this did not result in pla-
T W O TYPES OF A C I ' I N O P H A G E INFECTING S. scabies
2001
521
que formation, and a UV enrichment procedure had to be applied (Schneider et al. 199o). Irradiation by exposure to UV lamp (240 rim) and subsequent incubation were either carried out in the dark, or plates were irradiated and left on the bench exposed to laboratory illumination, for 89h prior to incubation in the dark at 28 ~ After 2 d, colonies were counted to obtain survival curves.
RESULTS AND DISCUSSION Isolation of phage-infected S. scabies MR13. Phage particles were detected in two out of the nine different soil samples irrigated with sewage water, and the phage plaques were obtained on S. scabies MR13 as indicator strain. Using differences in plaque morphology, size and lysogeny criteria, two different phages, termed dpS and ~bL, were identified, dpS and ~bL produced clear plaques on lawns of S. scabies MR13 (Fig. 1). The uniqueness of each phage was confirmed by morphological studies of the phage particles and the host-range determination. Some Streptomyces phages were partially characterized through their physico-chemical properties, plaque morphology, host range and particle morphology (Greene and Goldberg 1985; Rodriguez et al. x986; Diaz et al. I989; EI-Tarabily et al. I995; Ogiso et al. 1999). Morpholoyy of actinophage virions. Electron microscopic observations (Fig. 2) showed that the two types of actinophage virions had hexagonal heads and apparently noncontractile tails, q-he phage d?S had a long tail but the other type (dpL) had a short tail on the virions. Like nearly all previously characterized Streptomyces phages, the shape of the dpS (type I) virion was similar to that of ~bA3 and dpA8 (Diaz et al. I989). The ~bL (type II) virion was similar to that of dpSH-61 (Nishiwaki et al. I996) and of dpNC-4 (Ogiso et al. I999), with a hexagonal head and a relatively short thick tail. The two types of phages had a base plate at the end of the tail. The dimensions of the two phages are shown in Table I. The small phage (~bS) had a head of 100 nm from apex to apex and a tail 250 nm long. The head of the largest one (d~L) recorded was 212 nm but the length of the tail was 187 nm. The isolated phages are similar to other actinophages isolated by Diaz et al. (I989) and Ogiso et al. (I999).
Fig. 1. Plaques of dpS (lefO and d~L (right) on S. scabies MR13 after overnight.
Host range ofactinophages. The host range of the isolated phages was examined by plaque formation on 20 strains of pathogenic and nonpathogenic Streptomyces belonging to nine species. Each type of phage displayed a different host range (Table II) which varied from a relatively narrow one, as in the case of ~S (9 out of the 20 strains positive), to a wide one as in the case of ~L (14 hosts). The two actinophage isolates formed clear plaques against scab pathogens on S. scabies MR13, S-63 and S-64, except isolate S-64 which was not infected by ~bS. Among the nonpathogenic Streptomyces isolates, there were two types of phage-infected S. pluncolorescens SS3, S. plicatus SS5, S. cceruleorubidus SS10, S. albus SSll, S. nigellus SS12, S. fulvoviridis SS13 and S. spheroides SS17. On the other hand, none of the two phages infected S. sioyaensis SS1, S. pluricolorescens SS4, S. plicatus SS6 and SS7, S. coeruleorubidus SS9 and S. fulvoviridis SS16.
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Fig. 2. Electron micrographs of actinophages negatively stained with uranyl acetate; r/y/U: dpL. The bar represents 30 nm for r and 37.5 nm for ~L.
left: r
Table I. Morphological characteristics of the isolated Streptomyces phages r
Criteria
d~S
d~L
size, mm transparency edge
2-2.5 clear sharp
1-1.5 clear sharp
headt
apex to apex side to side
100 _+ 6 70 + 5
212 -+ 13 162 -+ 6
tailt
length width
250 _+ 11 8.0 +
187 -+ 5 18.0 +
Plaque morphology
Phage dimension, nm
Base plate$ tin
nm
(means
Table II. Actinophage (r
_+SD of at least 5 independent measurements).
S. sioyaensis S. pluricolorescens S. plicatus
* + -- presence of base plate.
and ~L) plaque formation on pathogenic and nonpathogenic Streptomyces isolatest
Isolate
S. scabies
and ~bL
r
d~L
MR13 S-63 S-64 SS1 SS2 SS3
+ + +
+ + + + +
554
--
--
SS5
+
+
556
--
--
SS7
-
-
-
Isolate
S. ceeruleorubidus
6S
d~L
-
S. albus S. niyellus S. fulvoviridis
SS8 SS9 SSIO SSll SS12 SS13 SS14 SS15 SS16
+ + + + -
+ + + + + + + -
S. spheroides
SS17
+
+
t ( + ) -- plaque formation, ( - ) -- no plaque formation.
The variation of the host range from a narrow to a wide activity spectra within the genus and strains of Streptomyces phages was demonstrated many times (Anne et al. I984; Greene and Goldberg x985; Diaz et al. I989; Hahn et a/. I99o; E1-Tarabily et al. I995; Balan and Padilla I997). The relationship between the concentration of the pathogens in soil and the occurrence of scab disease is not well established because there is no method for estimating the concentration of pathogens in soil. Ogiso et al. (I999) observed that actinophages of S. scabies are able to infect both pathogenic scab isolates and nonpathogenic Streptomyces spp.
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TWO TYPES OF ACTINOPHAGE INFECTING S. scabies
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Adsorption rate constant of isolated phages. Adsorption of dpS and ~bL was determined using S. scabies MR13 cells grown in phage medium to the early exponential phase of growth (15-h cultures). The phages were quickly adsorbed to the cells. About 77 and 74 % of all infective ~bS and d?L particles were adsorbed within 20 min of contact, respectively. The adsorption reached maximum after 32 min for both phages. The adsorption constant K was 3.44 pL/min for gbS and 3.18 pL/min for ~bL as determined by the formula K = 2.3/[Blt x log P0/P where
P0 P
[B] K
(Adams t959)
is phage assay at zero time phage not adsorbed at time t (min) concentration of bacteria (cells per mL) and velocity constant (mL/min).
One-step growth experiments indicated that ~bS and dpL log PFU/mL have a latent period of 30 min followed by a rise period of fur8 ther 30 rain (Fig. 3). The length of these periods is not exceptional, it is rather similar to those of many other actino-o j RP phages (Lomovskaya et al. i98o). "" I The mean of burst size was estiI I 0 30 60 mated to be 1.61 PFU/mL for rain ~bS and 3.75 PFU/mL for ~bL. Adsorption was, therefore, one Fig.3. One-stepgrowth curve of phages dpS (open symbols) and qbL (closed of the restricting factors. Anne et symboL,)development on S. scabies MR13; LP -- latent period, liP -- rise period. aL (I99O) found that efficient adsorption (>90 %) of VWB phage to S. venezuelae ETH 13640 and to S. exfoliatus was probably due to particular phage receptor protein at the cell surface of these strains. EI-Tarabily et al. (I995) found that the adsorption rate constants of the phage, ~bS1,dpS2and dpS3, was 1.58 x ! 0-7, 1.26 x 10-7 and 5.97 x 10-9 virions per cell, respectively. "[hey reported that the latent period value for the three phages was 35, 40 and 40 min, and the rise period of these phages was 40, 30 and 40 min, respectively. Determination of temperate phages and lysogenic isolates. Temperate phages could be recognized by the development of lysogenic Streptomyces isolates at the center of turbid plaques. Both phages on S. scabies MR13 formed clear plaques in this host. However, cells growing within the plaques were not immune to superinfection. Therefore, none of the two phages appeared to produce stable lysogenic derivatives in their original host. The temperate character of the two phages was tested in other Streptomyces isolates (Table II) in which they produced turbid plaques. The cells growing within these isolates were tested for reinfection of all bacterial lawns. Four phages formed stable lysogens in some of the tested isolates. According to spontaneous induction of free phage liberation and immunity to superinfection these phages were identified as temperate phages. Thus, ~bSS3was temperate in S. pluricolorescens SS3, dpSS12 in S. nigellus SS12 (dpS derivative), ~bSS13 in S. fulvoviridis SS13 and dpSS17was temperate in S. spheroides SS17 (gbLderivative). Cross immunity of the temperate phage and restriction barrier of lysogenic isolates. In order to study cross immunity of the temperate phages, it was necessary to find at least one or two host strains and/or isolates which could be infected and lysogenized by all temperate phages. The four temperate phages were tested for infection of lysogenic isolates by spotting high-titer phage suspensions (105-106 phages per spot). Thus, it was possible to use lysogenized isolates (S. pluricolorescens SS3, S. nigellus SS12, S.flavoviridis SS13 and S. spheroides SS17) for cross-immunity studies, revealing that dpSS3, ~bSS12 and dpSS13 are homoimmune whereas these phages are heteroimmune with respect to ~bSS17 (Table III). Lysogenic isolates of SS3, SS12, SS13 or SS17 containing dpSS3, ~bSS12, ~bSS13 or ~bSS17, respectively, were immune to superinfection by dpSS3, dpSS12, ~SS13 or dpSS17 obtained from their supernatants, respectively, but they were still susceptible to ~bSS3, ~bSS12, ~bSS13 or ~bSS17 propagated I0
LP
ij [
EI-S.A.EI-SAYED et al.
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on them. A similar result was reported on the i m m u n i t y a n d susceptibility of a lysogenic isolate of
Streptomyces by A n n e et al. ( i 984).
Table III. Cross immunity of the four phages and restriction barriers of derivative lysogenicisolates* Phages and isolates on which they were p/opagated Indicator ~SS3
di~SS12
~SS13
d/~SS17
isolates SS3. SS125 SS13~ SS175 SS3* SS127 SS13~ SS175 SS3~ SS12~ SS137 SS17~ SS3~ SS12$ SS135 SS17, SS3 SS12 SS13 SS17
-
+ + +
+ + -
+ + +
+ +
+ + + +
+ +
+ + +
+ +
+ + + +
+ + -
+ + +
+ +
+ + + +
+ + +
+ + +
*(+) - plaques were observed, (-) - no plaques observed (phage suspensions used in spot tests). 1'Phages (tl~SS3,~bSS12,~bSS13,t[~SS17)were obtained from supernatants of the corresponding lysogenicisolates. *Phages (dpSS3,d~SS12,~SS13, dbSS17)were propagated on SS12, SS13 or SS17.
The restriction systems of isolates (SS12, SS13 a n d SS17) have different specificity (Table III). Some propagations of phages (d/~SS3, dpSS12, dpSS13, ~bSS17) on these isolates did not form plaques, d~SS3 p r o p a g a t e d on SS12, SS13 or SS17 did not form plaques on SS12 and SS17, SS13 or SS12 a n d SS13, respectively. ~SS12 propagated on SS13 or SS17 did not form plaques o n SS13 or SS12 a n d SS13, respectively, a n d d?SS13 on SS12 or SS17 did not on SS12 a n d SS17 or SS12 a n d SS13, respectively. dpSS17 p r o p a g a t e d on SS12 or SS13 did not form them o n SS12 or SS13, respectively. These restriction barriers of SS12, SS13 a n d SS17 (lysogenic isolates) m a y interfere with cross-immunity of the t e m p e r a t e phages but could b e o v e r c o m e by applying a high phage titer. The r e s t r i c t i o n - m o d i f i c a t i o n systems were investigated in other streptomycetes by Chater and Wilde (I976), Chater a n d Carter (I979), a n d Schneider et al. 0 9 9 0 ) . O n the other hand, H a h n et al. (I99O) r e p o r t e d that actinophage FP22 a p p e a r e d to b e able to avoid restriction barriers in Streptomyces spp. a n d had a strong cross immunity.
Table IV. Photoreaction after UV treatment of SS12, SS13 and 5517 (survivingCFU, %)t Irradiation time 8
0 5 10 15 20 25 30 35 40 45 50
SS12 L
D
100 100 89 64 43 24 15 2.3 11 0.87 4.0 0.050 2.6 0.028 0.83 0.0095 0.35 0.0050 0.054 0.0093 0.015 0.00085
SS13 L/D 1.0 1.4 1.8 6.4 12 80 95 87 64 58 18
L 100 93 56 20 15 6.2 3.5 0.94 0.55 0.067 0.058
D 100 64 28 5.0 1.3 0.088 0.048 0.042 0.042 0.0045 0.0030
SS17 L/D 1.0 1.5 2.0 4.0 12 70 74 52 24 18 7.8
L
D
100 100 82 60 61 21 23 3.2 17 1.0 7.8 0.085 5.4 0.042 2.4 0.024 0.76 0.0089 0.065 0.0048 0.020 0.0032
L/D 1.0 1.4 2.7 7.5 16 91 128 101 85 13 6.2
tSpores were irradiated with UV and either extxx~d to laboratory illumination for 30 min prior to incubation in the dark (L), or directly incubated in the dark (D); L/D -- ratio L to D. The three host isolates (SS12, SS13, SS17) exhibited considerable restriction barriers for the t e m p e r a t e phages used. S p o n t a n e o u s transition from the t e m p e r a t e stage to the lyric cycle occurred at a rate of 1 - 5 % of the viable cell concentration ( A n n e et al. I984). Induction of the lytic cycle could be e n h a n c e d by exposure of the lysogenic isolates to U V t r e a t m e n t . C o m p a r i n g the dark a n d light survival
+ + + -
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TWO TYPES OF ACTINOPHAGE INFECTING S. scabies
525
results (Table IV), the irradiated isolates exhibited a photoreactivation system. "Ihus 30s of UV irradiation in the dark resulted in 0.028, 0.048 and 0.042 % survival, whereas 9'2 h subsequent exposure to laboratory illumination increased survival by 95-, 74-, and 128-fold for SS12, SS13 and SS17, respectively. Photoreactivation systems are widely distributed in bacteria and have also been reported for Streptomyces species (Parson I983; Hopwood et al. 1985; Schneider et al. s99o). Longer irradiation of the lysogenic isolates decreased the number of viable cells. The possible restriction barriers of the lysogenized derivatives of SS12, SS13 and SS17 had to ensure that they would not interfere with the cross-immunity studies and these barriers could be overcome after UV treatment of these isolates (data not shown). Similar results were obtained with S. ceelicolor DSM 40622 and DSM 40624 (Schneider et al. ~99o). Provided that the host strains have typical type II restriction endonucleases and corresponding methyltransferases, as is very common in Streptomyces (Cox and Baltz I984), it should be possible to mutate the endonuclease gene by UV irradiation in some spores without affecting the modification enzyme. Our results should not be limited to temperate phages and it would appear that d~S and dpL are good candidates for the development of cloning vectors: (i) they are temperate, a characteristic which would allow selection of cloned genes during the phage lysogenic cycle, and (ii) they are economically important, infecting scab pathogens. The authors are grateful to Dr. M. Mansour, Department of Food Hygiene, Faculty of Veterinary Medicine, Zagazig University, Zagazig (Egypt) for running some experiments in his laboratory.
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