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Mobilizable Rolling-Circle Replicating Plasmids from Gram-Positive Bacteria: A Low-Cost Conjugative Transfer

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  • Authors: Cris Fernández-López1, Alicia Bravo2, Sofía Ruiz-Cruz3, Virtu Solano-Collado4, Danielle A. Garsin5, Fabián Lorenzo-Díaz6, Manuel Espinosa7
  • Editors: Marcelo Tolmasky8, Juan Carlos Alonso9
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Centro de Investigaciones Biológicas, CSIC, Madrid, Spain 28040; 2: Centro de Investigaciones Biológicas, CSIC, Madrid, Spain 28040; 3: Centro de Investigaciones Biológicas, CSIC, Madrid, Spain 28040; 4: Centro de Investigaciones Biológicas, CSIC, Madrid, Spain 28040; 5: Department of Microbiology and Molecular Genetics, The University of Texas Health Science Center at Houston, Houston, Texas; 6: Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias, Universidad de La Laguna, Laguna, Spain 38071; 7: Centro de Investigaciones Biológicas, CSIC, Madrid, Spain 28040; 8: California State University, Fullerton, CA; 9: Centro Nacional de Biotecnología, Cantoblanco, Madrid, Spain
  • Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
  • Received 04 March 2014 Accepted 14 March 2014 Published 19 September 2014
  • Manuel Espinosa, mespinosa@cib.csic.es or Fabián Lorenzo-Díaz, florenzo@ull.edu.es
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  • Abstract:

    Conjugation is a key mechanism for horizontal gene transfer in bacteria. Some plasmids are not self-transmissible but can be mobilized by functions encoded provided by other auxiliary conjugative elements. Although the transfer efficiency of mobilizable plasmids is usually lower than that of conjugative elements, mobilizable plasmids are more frequently found in nature. In this sense, replication and mobilization can be considered important mechanisms influencing plasmid promiscuity. Here we review the currently available information on two families of small mobilizable plasmids from Gram-positive bacteria that replicate via the rolling-circle mechanism. One of these families, represented by the streptococcal plasmid pMV158, is an interesting model since it contains a specific mobilization module (MOB) that is widely distributed among mobilizable plasmids. We discuss a mechanism in which the promiscuity of the pMV158 replicon is based on the presence of two origins of lagging strand synthesis. The current strategies to assess plasmid transfer efficiency as well as to inhibit conjugative plasmid transfer are presented. Some applications of these plasmids as biotechnological tools are also reviewed.

  • Citation: Fernández-López C, Bravo A, Ruiz-Cruz S, Solano-Collado V, Garsin D, Lorenzo-Díaz F, Espinosa M. 2014. Mobilizable Rolling-Circle Replicating Plasmids from Gram-Positive Bacteria: A Low-Cost Conjugative Transfer. Microbiol Spectrum 2(5):PLAS-0008-2013. doi:10.1128/microbiolspec.PLAS-0008-2013.

Key Concept Ranking

Mobile Genetic Elements
0.8018963
Gene Expression and Regulation
0.71544194
Genetic Elements
0.5345975
Bacterial Diseases
0.4328259
Type IV Secretion Systems
0.41367048
0.8018963

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/content/journal/microbiolspec/10.1128/microbiolspec.PLAS-0008-2013
2014-09-19
2017-08-21

Abstract:

Conjugation is a key mechanism for horizontal gene transfer in bacteria. Some plasmids are not self-transmissible but can be mobilized by functions encoded provided by other auxiliary conjugative elements. Although the transfer efficiency of mobilizable plasmids is usually lower than that of conjugative elements, mobilizable plasmids are more frequently found in nature. In this sense, replication and mobilization can be considered important mechanisms influencing plasmid promiscuity. Here we review the currently available information on two families of small mobilizable plasmids from Gram-positive bacteria that replicate via the rolling-circle mechanism. One of these families, represented by the streptococcal plasmid pMV158, is an interesting model since it contains a specific mobilization module (MOB) that is widely distributed among mobilizable plasmids. We discuss a mechanism in which the promiscuity of the pMV158 replicon is based on the presence of two origins of lagging strand synthesis. The current strategies to assess plasmid transfer efficiency as well as to inhibit conjugative plasmid transfer are presented. Some applications of these plasmids as biotechnological tools are also reviewed.

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FIGURE 1

The MOB modules of plasmids pMV158 and pC221. The MOB cassette of pMV158, which contains a single gene encoding the MobM relaxase, is flanked by two s of the types U and A, respectively (see Fig. 2 ). In the case of pC221, there is a single (also termed ). Its MOB cassette contains three genes encoding the MobC, MobA, and MobB proteins. Relevant features of the s of plasmids pMV158 and pC221. The nucleotide sequences of the (coordinates 3564 to 3605) and (coordinates 3084 to 3160) are shown. The inverted repeats (IRs, arrows) and the nick site (, arrowhead) are indicated. Demonstrated minimal binding site for MobM (lined box), and MobA recognition site () and one of the MobC binding sites () are also specified. doi:10.1128/microbiolspec.PLAS-0008-2013.f1

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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FIGURE 2

Genetic organization of the MOB cassette in pMV158. Plasmid- and the gene are flanked by two lagging-strand origins of replication ( and ). Both s have the possibility of generating long hairpin-loop structures exhibited as “ssDNA promoters” ( 15 , 18 ) where the RNAP-binding site (RS) is recognized by the RNAP to synthesize a short RNA primer (pRNA). A consensus sequence (CS-6) located in the loop of the hairpin acts as the termination point for the pRNA synthesis. The pRNA is then used by DNA polymerase I for limited extension synthesis, followed by replication of the lagging strand by DNA Pol III. doi:10.1128/microbiolspec.PLAS-0008-2013.f2

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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FIGURE 3

Autoregulation of gene expression. The region of pMV158 that includes the and promoters of the gene is shown. In , transcription is mostly initiated from promoter (blue) ( 76 ). Promoter (black), which is located within the sequence, is used in ( 51 ). The main sequence elements of both promoters and the nick site () are indicated. Transcription start sites are also indicated with arrows. The regions recognized by MobM and RNA polymerase (RNAP) were determined by DNase I footprinting assays using linear double-stranded DNAs ( 42 , 76 ). MobM is able to repress the transcription initiated from both promoters, and ( 76 ). doi:10.1128/microbiolspec.PLAS-0008-2013.f3

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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FIGURE 4a

Expression of gene in cells harboring plasmid pMV158GFP. Phase-contrast and fluorescence microscopy of cells expressing after growth in sucrose (maltose promoter repressed in pneumococci; top panel) or in maltose ( induced; bottom panel) and cells expressing constitutive after growth in sucrose. See text for details. doi:10.1128/microbiolspec.PLAS-0008-2013.f4

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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FIGURE 4b

Expression of gene in cells harboring plasmid pMV158GFP. Phase-contrast and fluorescence microscopy of cells expressing after growth in sucrose (maltose promoter repressed in pneumococci; top panel) or in maltose ( induced; bottom panel) and cells expressing constitutive after growth in sucrose. See text for details. doi:10.1128/microbiolspec.PLAS-0008-2013.f4

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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FIGURE 5

OG1RF expressing green fluorescent protein (GFP) colonizes the intestine of . L4 larvae were exposed for 3 hours to OG1RF carrying plasmid pMV158GFP. Subsequently, worms were washed with M9 medium and anesthetized with 0.25 mM levamisol before imaging. DIC and fluorescence microscopy were used to visualize the worms. GFP expressing bacteria and auto-fluorescence generated by lipofuscin granules in the body of the worm were observed using FITC and DAPI filters, respectively. doi:10.1128/microbiolspec.PLAS-0008-2013.f5

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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FIGURE 6

Genetic maps of plasmid pLS1 (a nonmobilizable pMV158 replicon) and its derivatives pAST, pAST-, and pAST- ( 128 ). Only relevant features are indicated. and genes are involved in plasmid DNA replication. The location of the replication origins (double-strand origin) and (single-strand origin) is indicated. The gene confers resistance to tetracycline. T1T2, tandem terminators and of the rRNA operon; SD, translation initiation signals optimized for the expression of the gene in prokaryotes ( 114 ). The positions of the and promoters are indicated. , III; , I; B, HI; , I; , I. doi:10.1128/microbiolspec.PLAS-0008-2013.f6

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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FIGURE 7

Strategy for high-throughput plasmid transfer detection. Plasmid-containing donor (D) and recipient (R) cells are mixed (it can be done at different ratios), filtered in a 96-filter-well plate (0.22 µm), and placed on a layer of solid conjugation medium (containing 5 µg/ml DNase I). After 4 h at 37°C, selection for transconjugants (T) is applied by adding antibiotic-containing medium and application of gentle vacuum. Thus, for each well the transfer frequencies can be assessed by a number of methods, such as plating on selective medium, fluorescent confocal microscopy (-expressing plasmids), LacZ measurements, or quantitative PCR. (Modified from Lorenzo-Díaz F, Espinosa M, 2009. Large-scale filter mating assay for intra- and inter-specific conjugal transfer of the promiscuous plasmid pMV158 in Gram-positive bacteria. 65–70 [ 123 ]. Copyright 2009, with permission from Elsevier.) doi:10.1128/microbiolspec.PLAS-0008-2013.f7

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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Tables

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TABLE 1

RCR-plasmids from Gram-positive bacteria belonging to the MOB family

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013
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TABLE 2

Indicators of pMV158 promiscuity: relative efficiencies of conjugative transfer from donor to recipients and

Source: microbiolspec September 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0008-2013

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