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The Plasmid Mobilome of the Model Plant-Symbiont : Coming up with New Questions and Answers

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  • Authors: Antonio Lagares1, Juan Sanjuán2, Mariano Pistorio3
  • Editors: Marcelo E. Tolmasky4, Juan Carlos Alonso5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: IBBM, Instituto de Biotecnología y Biología Molecular, CONICET - Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, (1900) La Plata, Argentina; 2: Departamento de Microbiología del Suelo y Sistemas Simbióticos. Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Granada, Spain; 3: IBBM, Instituto de Biotecnología y Biología Molecular, CONICET - Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, (1900) La Plata, Argentina; 4: California State University, Fullerton, CA; 5: Centro Nacional de Biotecnología, Cantoblanco, Madrid, Spain
  • Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0005-2013
  • Received 21 April 2014 Accepted 23 May 2014 Published 24 October 2014
  • Antonio Lagares, lagares@biol.unlp.edu.ar
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  • Abstract:

    Rhizobia are Gram-negative Alpha- and Betaproteobacteria living in the underground which have the ability to associate with legumes for the establishment of nitrogen-fixing symbioses. in particular—the symbiont of , , and spp.—has for the past decades served as a model organism for investigating, at the molecular level, the biology, biochemistry, and genetics of a free-living and symbiotic soil bacterium of agricultural relevance. To date, the genomes of seven different strains have been fully sequenced and annotated, and several other draft genomic sequences are also available. The vast amount of plasmid DNA that frequently bears (up to 45% of its total genome), the conjugative ability of some of those plasmids, and the extent of the plasmid diversity has provided researchers with an extraordinary system to investigate functional and structural plasmid molecular biology within the evolutionary context surrounding a plant-associated model bacterium. Current evidence indicates that the plasmid mobilome in is composed of replicons varying greatly in size and having diverse conjugative systems and properties along with different evolutionary stabilities and biological roles. While plasmids carrying symbiotic functions (pSyms) are known to have high structural stability (approaching that of chromosomes), the remaining plasmid mobilome (referred to as the non-pSym, , or compartment) has been shown to possess remarkable diversity and to be highly active in conjugation. In light of the modern genomic and current biochemical data on the plasmids of , the current article revises their main structural components, their transfer and regulatory mechanisms, and their potential as vehicles in shaping the evolution of the rhizobial genome.

  • Citation: Lagares A, Sanjuán J, Pistorio M. 2014. The Plasmid Mobilome of the Model Plant-Symbiont : Coming up with New Questions and Answers. Microbiol Spectrum 2(5):PLAS-0005-2013. doi:10.1128/microbiolspec.PLAS-0005-2013.

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2014-10-24
2017-06-27

Abstract:

Rhizobia are Gram-negative Alpha- and Betaproteobacteria living in the underground which have the ability to associate with legumes for the establishment of nitrogen-fixing symbioses. in particular—the symbiont of , , and spp.—has for the past decades served as a model organism for investigating, at the molecular level, the biology, biochemistry, and genetics of a free-living and symbiotic soil bacterium of agricultural relevance. To date, the genomes of seven different strains have been fully sequenced and annotated, and several other draft genomic sequences are also available. The vast amount of plasmid DNA that frequently bears (up to 45% of its total genome), the conjugative ability of some of those plasmids, and the extent of the plasmid diversity has provided researchers with an extraordinary system to investigate functional and structural plasmid molecular biology within the evolutionary context surrounding a plant-associated model bacterium. Current evidence indicates that the plasmid mobilome in is composed of replicons varying greatly in size and having diverse conjugative systems and properties along with different evolutionary stabilities and biological roles. While plasmids carrying symbiotic functions (pSyms) are known to have high structural stability (approaching that of chromosomes), the remaining plasmid mobilome (referred to as the non-pSym, , or compartment) has been shown to possess remarkable diversity and to be highly active in conjugation. In light of the modern genomic and current biochemical data on the plasmids of , the current article revises their main structural components, their transfer and regulatory mechanisms, and their potential as vehicles in shaping the evolution of the rhizobial genome.

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FIGURE 1

Scheme of the different possible destinies of the model plasmid pSmeLPU88b::Tn5 when transferred to from different plasmid-diversity groups (plasmid OTU types; see reference 13 ). The percentage assigned to each event was calculated upon consideration of an abundance of plasmid OTU types in which all are equally represented. Box A represents those OTUs that proved unable to host plasmid pSmeLPU88b::Tn5 because of either surface-exclusion phenomena or plasmid restriction within the recipient cell. Box B represents OTUs bearing helper functions able to mobilize the model plasmid. Box C represents isolates that, under our experimental conditions, were not able to mobilize plasmid pSmeLPU88b::Tn5. Some isolates belonging to the helper (+) class (Box B) or the helper (–) class (Box C) bear cryptic plasmids that display a replication incompatibility with plasmid pSmeLPU88b::Tn5 (dotted box). CRY, cryptic plasmid. The percent values on the right denote the maximal expected transfer frequency to a third bacterial strain (Reprinted from [ 13 ] with permission of the publisher). doi:10.1128/microbiolspec.PLAS-0005-2013.f1

Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0005-2013
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FIGURE 2

Phylogenetic (neighbor-joining) tree showing the relationships between different relaxases of the MOB cluster as inferred from their complete protein sequences. The bootstrap-consensus tree inferred from 1,000 replicates is taken to represent the evolutionary history of the proteins (corresponding to the indicated taxa) analyzed ( 80 ). The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. The tree is drawn to scale, with the branch lengths in proportion to the evolutionary distances used to construct the phylogenetic tree. Those distances were computed by means of the Poisson-correction method ( 81 ) with the units being the number of amino acid substitutions per site. The protein sequences used were obtained from GenBank under the accession numbers indicated in parentheses before the name of each plasmid replicon. The box over the tree indicates the clades that include the close MOB, MOB, and MOB families of relaxases. *See text for description of type IV Dtrs. The black dots denote those plasmid replicons that bear nodulation () genes (Reprinted from [ 67 ] with permission of the publisher). doi:10.1128/microbiolspec.PLAS-0005-2013.f2

Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0005-2013
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FIGURE 3

Proposed model for the regulation of conjugative transfer of the symbiotic plasmids. (A) Under nonfavorable conditions (i.e., standard laboratory media), RctR silences the Sma0953/50- and SMa0956-58-59- operons, so that remains inactive and RctA represses conjugative transfer in both pSyms. (B) Conjugative transfer is achieved after an unknown compound—putatively imported by the ABC transporter encoded by SMa0953-50 and modified by the SMa0956-58-59 gene products—binds RctR, thereby relieving transcription repression of . The resulting transcription ends up with the activation of to counteract RctA, the conjugative-transfer operons become expressed, and plasmid conjugation is able to proceed. (+) activation; (–) repression or inhibition; BM, bacterial membrane (Reprinted from [ 59 ] with permission of the publisher). doi:10.1128/microbiolspec.PLAS-0005-2013.f3

Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.PLAS-0005-2013
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