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Applied and Environmental Microbiology, February 2000, p. 529-534, Vol. 66, No. 2
Center of Marine Biotechnology, University of
Maryland Biotechnology Institute, Baltimore, Maryland
21202,1 and Department of Biological
Sciences, University of Warwick, Coventry, West Midlands CV4 7AL,
United Kingdom2
Received 12 August 1999/Accepted 29 September 1999
The interspecific transfer of two giant linear plasmids was
investigated in sterile soil microcosms. Plasmids pRJ3L (322 kb) and
pRJ28 (330 kb), both encoding mercury resistance, were successfully transferred in amended soil microcosms from their streptomycete hosts,
the isolates CHR3 and CHR28, respectively, to a plasmidless and
mercury-sensitive strain, Streptomyces lividans TK24.
Transconjugants of S. lividans TK24 were first observed
after 2 to 3 days of incubation at 30°C, which corresponded to the
time taken for the formation of mycelia in soil. Transfer frequencies
were 4.8 × 10 Streptomycetes are common
inhabitants of the soil environment and are regarded as the most
numerous actinomycetes isolated from soil (31).
Predominantly found as spores, streptomycetes can germinate and grow
into a mycelial state for brief periods of time when nutrients become
available (19). The growth of streptomycetes in soil is
discontinuous in space and time, and survival between brief periods of
vegetative growth is by production of spores resistant to starvation
and desiccation (30, 31). Streptomyces species
can survive for several weeks in sterile and nonsterile soil as spores
after a short mycelial growth phase of 2 to 3 days (28).
Under these conditions, the covalently closed circular plasmid pIJ673
was transferred intra- or interspecifically in sterile and nonsterile
soil (28). The detection of transconjugants correlated with
the mycelial stage of both the donor and recipient (28).
Plasmid transfer between streptomycetes in soil has been well studied
(2, 22, 27-29), and a mathematical model for the transfer
of covalently closed circular plasmids in soil microcosms has been
deduced, taking into account the reduction in the exponential growth
rate due to depletion of nutrients and/or moisture from soil
microcosms, important factors influencing the development of
streptomycetes in soil (5). However, there are no reports of
transfer of Streptomyces giant linear plasmids in soil
microcosms. Linear plasmids were first described in
Streptomyces spp. by Hayakawa et al. (9), and
studies by Kinashi and coworkers (16, 17) have demonstrated
the presence of giant linear plasmids (>100 kb) in several
antibiotic-producing Streptomyces spp. Linear plasmids ranging in size from 12 kb to 1 Mb have now been reported in more than
10 Streptomyces spp. (4, 8, 10, 32, 34), and they
have also been found in other actinomycete genera such as Nocardia, Rhodococcus, and
Mycobacterium (6, 12, 13, 21). Giant linear
plasmids confer advantageous phenotypes and have been shown to carry
genes encoding antibiotic biosynthesis, resistance to heavy metals, and
ability to break down xenobiotics (for a review, see reference
20). At the molecular level, some linear plasmids
have been shown to integrate into the chromosome, existing as an
integrated or a free form (18). Recently, we demonstrated that mercury resistance genes were located on transmissible giant linear plasmids in two Chesapeake Bay Streptomyces isolates
(24). This finding has important ecological implications, as
plasmid transfer might be responsible for the spread of mercury
resistance genes in polluted environments. Transfer functions of linear
plasmids are still unknown. However, Zotchev and Schrempf
(33) have cloned a 5.74-kb region of pBL1, a 43-kb
Streptomyces linear plasmid, containing at least five open
reading frames ORFs necessary for plasmid transfer and regulation.
Using two well-characterized Streptomyces strains (23,
24), we studied the transfer of two giant linear plasmids
encoding mercury resistance, pRJ3L (322 kb) and pRJ28 (330 kb), between their respective hosts, Streptomyces strains CHR3 and CHR28
and a mercury-sensitive laboratory strain, S. lividans TK24,
in amended sterile soil microcosms. We report the first example of
transfer of giant linear plasmids in soil microcosms and compare
transfer frequencies and time scales of initial transfer with those
found with the covalently closed circular plasmid pIJ673
(28). In addition, we show that large
Streptomyces plasmids encoding mercury resistance are
widespread in mercury-contaminated sediments.
Bacterial strains and plasmids.
The strains used in plasmid
transfer experiments are described in Table
1. All strains were maintained as spores
prepared on solid agar ISP Medium 2 (YME) (Difco Laboratories, Detroit, Mich.) incubated at 30°C, as described by Hopwood et al.
(11). Streptomyces strains were isolated from
mercury-contaminated sediments in Boston Harbor (3),
Townsville Harbor, Australia (7), and the Sali River,
Tucuman, Argentina (1), by our previously described
isolation procedure (23).
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Copyright © 2000, American Society for Microbiology. All rights reserved.
Interspecific Transfer of Streptomyces
Giant Linear Plasmids in Sterile Amended Soil Microcosms
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
4 and 3.6 × 105
CFU/donor genome for pRJ3L and pRJ28, respectively. Transconjugants were analyzed by pulsed-field gel electrophoresis for the presence of
plasmids, and plasmid identity was confirmed by restriction digests.
Total genomic DNA digests confirmed that transconjugants were S. lividans TK24. The mercury resistance genes were shown to be on
the plasmid in the transconjugants by hybridization analysis and were
still functional. This is the first demonstration of transfer of giant
linear plasmids in sterile soil microcosms. Giant linear plasmids were
detected in many Streptomyces spp. isolated from
mercury-contaminated sediments from Boston Harbor (United States),
Townsville Harbor (Australia), and the Sali River (Tucuman, Argentina).
Mercury resistance genes were shown to be present on some of these
plasmids. Our findings that giant linear plasmids can be transferred
between Streptomyces spp. and are common in environmental
Streptomyces isolates suggest that these plasmids are
important in gene transfer between streptomycetes in the environment.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
TABLE 1.
Bacterial strains and plasmids used in this study
Soil microcosm experiments. The soil used in this study was taken from a local wheat field site at Cryfield, University of Warwick, Coventry, United Kingdom. Soil was prepared as previously described (28). Soil subsamples (10 g in 50 ml-Universal glass vials) were amended with 1% (wt/wt) soluble starch (Sigma Chemical Co., St. Louis, Mo.) and 1% (wt/wt) crabshell chitin (Sigma) prior to sterilization at 121°C for 15 min. Separate duplicate microcosms were prepared for sacrificial sampling at each time point. Spores were counted directly by microscopy and by plating in triplicate onto YME plus chloramphenicol (25 µg/ml) or mercuric chloride (0.05 mM). Inocula consisted of a mixture of donor and recipient spores in sufficient distilled water to give a final moisture content of 15% (wt/wt) in the microcosms. The donor-to-recipient ratio was 1:5 (105 spores of donor) in all experiments. Microcosms were incubated at 30°C. Spores and mycelia were extracted with one-fourth-strength Ringer solution (0.6 mM NaHCO3, 39 mM NaCl, 1.4 mM KCl, 1.6 mM CaCl2) by shaking 1 g of soil in 2 ml of solution on a Griffin flask shaker for 10 min. Appropriate dilutions prepared in one-fourth-strength Ringer solution were plated onto three selective media and incubated at 30°C: (i) YME agar containing 0.01 mM HgCl2 (selection of donor); (ii) YME agar containing 25 µg of chloramphenicol (selection of recipient) per ml; and (iii) YME agar containing 0.01 mM HgCl2 and 25 µg of chloramphenicol (selection of transconjugants) per ml. All experiments were carried out in duplicate, and samples taken at each time point were plated in triplicate.
PFGE.
DNA plug preparation, plasmid restriction digests, and
pulsed-field gel electrophoresis (PFGE) analysis were performed as described previously (24). Ramping times are indicated in
the legends of Fig. 2 to 4. Ladders of 
DNA concatamers and
Saccharomyces cerevisiae YNN 295 chromosomes (Bio-Rad
Laboratories) were used as molecular weight standards. DNA was stained
with SYBR Green I (Molecular Probes, Inc., Eugene, Oreg.) prior to
photography with 302-nm UV light illumination by using a SYBR Green I
gel stain photographic filter (Molecular Probes, Inc.). The gels were digitized by using a FluorImager 573 (Molecular Dynamics,
Sunnyvale, Calif.).
DNA labeling and Southern hybridization. An 816-bp PvuII fragment (MER-A) of the S. lividans 66 mercuric reductase gene merA and a 716-bp SalI-EcoRV fragment (MER-B) of the organomercurial lyase gene merB were prepared from plasmid pJOE851.2 (25), kindly donated by J. Altenbuchner, Stuttgart, Germany. Probes were labeled and Southern hybridizations were performed as described previously (23).
Determination of mercury resistance by agar diffusion assay. Sensitivity of strains to mercury was tested by agar diffusion assay (26), as described previously (24).
Plasmid curing by growth at elevated temperature. Streptomyces strains CHR3 and CHR28 were cultured in YME and incubated with shaking (300 rpm) at 30, 42, and 45°C for 48 h. Mycelia were collected and PFGE plugs were prepared and digested with restriction enzymes AseI as described previously (24).
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RESULTS AND DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Streptomyces species isolated from the marine environment and carrying plasmid-borne mercury resistance were found to survive in soil and transfer mercury resistance. Transfer of two giant linear plasmids pRJ3L and pRJ28 (322 and 330 kb in size, respectively) was observed. Both plasmids are well characterized (24) and were used to estimate the extent of giant linear plasmid transfer in soil and to determine the time scale of the initial transfer in soil microcosms.
Transfer frequencies and growth curves. Spores and mycelia were extracted from soil microcosms, and appropriate dilutions were plated on three selective media for enumeration of donors (CHR3 or CHR28), recipient S. lividans TK24, and transconjugants. Plate counts are shown in Fig. 1. Transconjugants were detectable at days 2 and 3 for pRJ3L and pRJ28, respectively. The numbers of transconjugants then increased exponentially until day 4, followed by a slower rate of increase from day 7 to 14 (1.9 × 106 CFU/g for CHR3T and 1.2 × 105 CFU/g for CHR28T after 14 days) (Fig. 1). This profile is in agreement with earlier observations made with a small covalently closed circular plasmid pIJ673 for transfer in soil microcosms (28) and described by Clewlow et al. (5) in a mathematical model of plasmid transfer between strains of streptomycetes in soil microcosms. In the model, donors and recipient grew exponentially up to ca. day 7, after which competition for nutrients and/or decreasing moisture levels began to result in a reduced growth rate. Transconjugants formed during a period of plasmid transfer from day 0 to day 2, suggesting that mycelial growth and contact were necessary for plasmid transfer. After day 2, transconjugants grew exponentially until day 7 where growth rate reduction occurred, as for the donor and recipient populations. Successful plasmid transfer is unlikely to occur after 7 days under these poor growth conditions. Rate parameters for the model were obtained from experiments done with Warwick soil, and similar methods were applied in this study. In general, the fit of this model was good for plasmid pIJ673, and similar trends were observed in the present study. Nutrient and moisture depletion are likely to have had a similar effect on giant linear plasmid transfer.
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), recipient S. lividans TK24
(
), and transconjugants (
) are as marked. Plate counts are the
results from duplicate microcosms (triplicate plating), and the
standard errors are indicated.
4 and
3.6 × 105 CFU/donor genome for CHR3 and CHR28,
respectively. These frequencies of transfer were similar to those found
with the covalently closed circular plasmid pIJ673, which transferred
interspecifically with an efficiency of 7.4 × 104
CFU/donor genome (28). We previously found transfer
frequencies of 1.5 × 102 and 1.8 × 103 transconjugants per donor genome for CHR3 and CHR28,
respectively, in plasmid transfer experiments on agar plates
(24). Mechanisms of transfer of giant linear plasmids are
not well understood. The similarities in rate and frequency of transfer
of covalently closed circular and giant linear plasmids in sterile soil
suggest that a similar mechanism may be present in both cases. For
covalently closed circular plasmid transfer, an initial mycelial
contact was necessary, followed by mycelial fusion upon which transfer occurs. This was followed by spreading of plasmids into the mycelial mass (14, 15). At present, the tra genes on giant
linear plasmids are not known, and it will be interesting to determine
whether they are homologous to the plasmid transfer genes in covalently closed circular plasmids (14, 15).
Confirmation of transconjugants. Colonies growing on YME containing 0.01 mM HgCl2 and chloramphenicol (25 µg/ml) were considered as transconjugants and were transferred individually onto fresh YME plates containing the same concentration of mercuric chloride and chloramphenicol to confirm their phenotypic traits. All transconjugants tested maintained growth after subculture on YME containing HgCl2 and chloramphenicol. Moreover, transconjugants recovered from the different crosses showed the characteristic gray spore color of S. lividans TK24, easily distinguishable from the white spores of Streptomyces sp. strain CHR3 and the dark green spores of Streptomyces sp. strain CHR28.
In order to compare the resistance of transconjugants and donors to mercury, one transconjugant of each cross from time points of 3, 7, and 14 days was analyzed by agar diffusion disk assay for HgCl2 and phenylmercuric acetate resistance (results not shown). No differences in mercury resistance profiles were observed between the original donors (CHR3 and CHR28) and the three transconjugants tested for each donor. To confirm the transfer of the plasmids as nonintegrative elements, transconjugants from microcosms sampled at days 3, 7, and 14 were analyzed by PFGE (Fig. 2A). A plasmid of identical size to pRJ28 (330 kb) was present in each transconjugant. Crosses between CHR3 and S. lividans TK24 gave transconjugants that contained only one plasmid of identical size to pRJ3L (322 kb). No plasmid bands corresponding in size to pRJ3H were observed in transconjugants. pRJ3H does not encode mercury resistance (24), and therefore there would be no selection for transconjugants containing pRJ3H under these experimental conditions (i.e., on mercury-containing media). Transfer of pRJ3H is therefore unlikely to be detectable in these experiments and may or may not have occurred. The original donor strains, sampled at day 14, retained their original plasmids (pRJ28 in strain CHR28, pRJ3H and pRJ3L in strain CHR3). No plasmids were present in mercury-sensitive S. lividans TK24 after 14 days in soil microcosms. Hybridization with probes MER-A (Fig. 2B) and MER-B (Fig. 2C) confirmed the presence of the mercury resistance genes on the plasmids present in transconjugants. Also, mercury resistance genes were located on plasmids pRJ3L and pRJ28 in the two original donor strains (CHR3 and CHR28, respectively) and in the donor strains sampled at 14 days. Both probes hybridized with the plasmids in each transconjugant but not with the chromosomal DNA of transconjugants (Fig. 2B and C).
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Interspecific transfer and curing experiments. The transfer described here between Streptomyces sp. strains CHR3 or CHR28 and S. lividans TK24 is interspecific. 16S rRNA sequencing (23) clearly showed that both Streptomyces CHR3 and CHR28 are closely related to, although not necessarily the same species as, S. rochei, whereas the recipient in this experiment was S. lividans. No plasmidless strains of CHR3 or CHR28 were available. Multiple rounds (thirty) of sporulation/ germination on rich media were unsuccessful in curing the plasmids, as reported previously (24). In another attempt to cure plasmids pRJ3L and pRJ28, CHR3 and CHR28 were cultured at elevated temperatures (42 and 45°C). The plasmid band intensity of pRJ3L was dramatically reduced when Streptomyces sp. strain CHR3 was grown at 45°C (Fig. 3A). However, plasmid pRJ3H band intensity remained similar at 30, 42, and 45°C (Fig. 3A). Digestion of total genomic DNA with AseI, which cuts pRJ3L once, also showed reduced intensity of both pRJ3L restriction fragments indicated by the arrows in Fig. 3B. Growth at 42°C did not change band intensity of pRJ3L (Fig. 3A and B) or pRJ28 (data not shown). Streptomyces sp. strain CHR28 did not grow at 45°C, and CHR3 did not grow at temperatures higher than 45°C. Hybridization with probe MER-A confirmed the presence of pRJ3L in CHR3 grown at 45°C, and this probe did not hybridize to any chromosomal bands, indicating that pRJ3L had not integrated into the chromosome (Fig. 3C). After plating of the culture grown at 45°C on YME plates without mercury selection, subculturing of 300 individual clones gave colonies that were all mercury resistant. We were unsuccessful in curing pRJ28 or pRJ3L, making it impossible to examine the intraspecific transfer of linear plasmids in soil microcosms. The fact that all colonies tested after culture at elevated temperature retained mercury resistance suggests that there was an overall reduction in copy number rather than persistence of plasmid copies in only part of the population.
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Widespread occurrence of Streptomyces giant linear plasmids encoding mercury resistance. Twenty-nine Streptomyces strains isolated from highly mercury contaminated Boston Harbor sediment samples (3) were screened for the presence of giant linear plasmids. Overall, 20 of these strains contained one or more giant linear plasmids, ranging in size between ca. 50 and 600 kb. Five strains contained two plasmids. Hybridization with probe MER-A confirmed that 18 of the total of 25 giant linear plasmids encoded mercury resistance. A set of the giant linear plasmids detected in Boston Harbor Streptomyces isolates is shown in Fig. 4A. Of 12 Streptomyces isolates from the Sali River, Argentina, 7 contained giant linear plasmids ranging in size from ca. 60 to 400 kb, 1 of which encoded mercury resistance as indicated by hybridization with the MER-A gene probe (Fig. 4B). Three of nine Streptomyces strains from Townsville Harbor, Australia, contained giant linear plasmids ranging from ca. 50 to 300 kb, two of which showed homology to merA (Fig. 4C).
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ACKNOWLEDGMENTS |
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This study was supported by the Schering-Plough Research Institute.
We thank Ann Horan for her support and Frank Robb for comments on the manuscript. We thank Michael Bothner and Maria Amoroso for supplying sediments from Boston Harbor and from the Sali River, Argentina, respectively.
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FOOTNOTES |
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* Corresponding author. Mailing address: Center of Marine Biotechnology, University of Maryland Biotechnology Institute, Columbus Center Suite 236, 701 East Pratt St., Baltimore, MD 21202. Phone: (410) 234-8883. Fax: (410) 234-8896. E-mail: hillr{at}umbi.umd.edu.
Contribution no. 500 from the Center of Marine Biotechnology.
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Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Applied and Environmental Microbiology, February 2000, p. 529-534, Vol. 66, No. 2
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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