A Common Genomic Framework for a Diverse Assembly of Plasmids in the Symbiotic Nitrogen Fixing Bacteria

The Wellcome Trust Sanger Institute, Hinxton, Cambridge, United Kingdom.
PLoS ONE (Impact Factor: 3.53). 02/2008; 3(7):e2567. DOI: 10.1371/journal.pone.0002567
Source: PubMed Central

ABSTRACT This work centres on the genomic comparisons of two closely-related nitrogen-fixing symbiotic bacteria, Rhizobium leguminosarum biovar viciae 3841 and Rhizobium etli CFN42. These strains maintain a stable genomic core that is also common to other rhizobia species plus a very variable and significant accessory component. The chromosomes are highly syntenic, whereas plasmids are related by fewer syntenic blocks and have mosaic structures. The pairs of plasmids p42f-pRL12, p42e-pRL11 and p42b-pRL9 as well large parts of p42c with pRL10 are shown to be similar, whereas the symbiotic plasmids (p42d and pRL10) are structurally unrelated and seem to follow distinct evolutionary paths. Even though purifying selection is acting on the whole genome, the accessory component is evolving more rapidly. This component is constituted largely for proteins for transport of diverse metabolites and elements of external origin. The present analysis allows us to conclude that a heterogeneous and quickly diversifying group of plasmids co-exists in a common genomic framework.

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Available from: Santiago Castillo-Ramírez, Aug 14, 2015
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    • "that are highly expressed by rhizobia on plant roots [33]. On the other hand, plasmids are highly variable and confer adaptive traits, such as nodulation and nitrogen fixation in legumes [6] [8] [19] [26] [29] [38] [43] [49] [51], or they may be transferred between bacteria [30] [31] [40]. "
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    ABSTRACT: Genomics has provided data for defining bacterial-species limits from estimates of gene conservation, synteny, average nucleotide identity (ANI) and in silico DNA-DNA hybridization (DDH). Phylogenomic analyses that allowed a more accurate definition of rhizobial relationships showed two major superclades within the family Rhizobiaceae that corresponded to the Rhizobium/Agrobacterium and Shinella/Ensifer groups. Within the Rhizobium/Agrobacterium group, four highly-supported clades were evident that could correspond to distinct genera. The Shinella/Ensifer group encompassed not only the genera Shinella and Ensifer but also a separate clade containing the type strain of R. giardinii. Ensifer adhaerens (Casida AT) was an outlier within its group, separated from the rest of the Ensifer (formerly Sinorhizobium) strains. The phylogenomic analysis presented provided support for the revival of Allorhizobium as a bona fide genus within the Rhizobiaceae, the distinctiveness of Agrobacterium and the recently proposed Neorhizobium genus, and suggested that R. giardinii may be transferred to a novel genus. ANI reference values are becoming the gold standard in rhizobial taxonomy and are being used to recognize novel rhizobial lineages and species that seem to be biologically coherent, as shown in this study.
    Systematic and Applied Microbiology 12/2014; 38(4). DOI:10.1016/j.syapm.2014.12.002 · 3.31 Impact Factor
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    • "In contrast to chromosomes , plasmids are considered as usually poorly conserved, flexible and heterogeneous in size and gene content. Variations in the location of chromosomal and extrachromosomal genes can be observed even in small rhizobial populations (Crossman et al. 2008; Mazur et al. 2011b; López-Guerrero et al. 2012). Some of the rhizobial extrachromosomal replicons referred to as chromids are characterised by a plasmid-type replication system but differ from plasmids in their GC content and codon usage, which are similar to those of the chromosome. "
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    ABSTRACT: Rhizobium leguminosarum bv. trifolii TA1 (RtTA1) is a soil bacterium establishing a highly specific symbiotic relationship with clover, which is based on the exchange of molecular signals between the host plant and the microsymbiont. The RtTA1 genome is large and multipartite, composed of a chromosome and four plasmids, which comprise approximately 65 % and 35 % of the total genome, respectively. Extrachromosomal replicons were previously shown to confer significant metabolic versatility to bacteria, which is important for their adaptation in the soil and nodulation competitiveness. To investigate the contribution of individual RtTA1 plasmids to the overall cell phenotype, metabolic properties and symbiotic performance, a transposon-based elimination strategy was employed. RtTA1 derivatives cured of pRleTA1b or pRleTA1d and deleted in pRleTA1a were obtained. In contrast to the in silico predictions of pRleTA1b and pRleTA1d, which were described as chromid-like replicons, both appeared to be completely curable. On the other hand, for pRleTA1a (symbiotic plasmid) and pRleTA1c, which were proposed to be unessential for RtTA1 viability, it was not possible to eliminate them at all (pRleTA1c) or entirely (pRleTA1a). Analyses of the phenotypic traits of the RtTA1 derivatives obtained revealed the functional significance of individual plasmids and their indispensability for growth, certain metabolic pathways, production of surface polysaccharides, autoaggregation, biofilm formation, motility and symbiotic performance. Moreover, the results allow us to suggest broad functional cooperation among the plasmids in shaping the phenotypic properties and symbiotic capabilities of rhizobia. Electronic supplementary material The online version of this article (doi:10.1007/s13353-014-0220-2) contains supplementary material, which is available to authorized users.
    Journal of applied genetics 05/2014; DOI:10.1007/s13353-014-0220-2 · 1.90 Impact Factor
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    • "Several examples, particularly in the Rhizobiaceae family, demonstrate that a substantial portion of the existing genetic diversity is plasmid determined, where isolates of the same or closely related species share the same genomic core with plasmid-concentrated variation (Schofield et al. 1987; Gonzalez et al. 2003; Cervantes et al. 2011; Perez-Segura et al. 2013). One study compared isolates of two Rhizobium species and found that accessory plasmids were related by syntenic blocks of sequence, suggestive of high levels of recombination and genomic rearrangements within and between plasmids (Crossman et al. 2008). Similarly, a genome comparison between the two species A. tumefaciens C58 and Agrobacterium sp. "
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    ABSTRACT: The accessory plasmid pAtC58 of the common laboratory strain of Agrobacterum tumefaciens confers numerous catabolic functions and has been proposed to play a role in virulence. Genomic sequencing of evolved laboratory strains of A. tumefaciens revealed the presence of multiple deletion events in the At plasmid, with reductions in plasmid size ranging from 25-30% (115 kb-194 kb). Flanking both ends of the sites of these deletions is a short-nucleotide repeat sequence that is in a single copy in the deleted plasmids, characteristic of a phage or transposon mediated deletion event. This repeat sequence is widespread throughout the C58 genome, but concentrated on the At plasmid, suggesting its frequency to be non-random. In this study, we assess the prevalence of the larger of these deletions in multiple C58 derivatives and characterize its functional significance. We find that in addition to elevating virulence gene expression, this deletion is associated with a significantly reduced carriage cost to the cell. These observations are a clear demonstration of the dynamic nature of the bacterial genome and suggest a mechanism for genetic plasticity of these costly but otherwise stable plasmids. Additionally, this phenomenon could be the basis for some of the dramatic recombination events so ubiquitous within and among megaplasmids.
    Genome Biology and Evolution 06/2013; 5(7). DOI:10.1093/gbe/evt095 · 4.53 Impact Factor
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