Plasmids impact on rhizobia-legumes symbiosis in diverse environments

Zahran, H. H.

doi:10.1007/s13199-017-0476-5

Cited by 15 publications

(11 citation statements)

References 226 publications

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“…The distribution of accessory genes (including the symbiotic genes) in the 55 complete genomes of Rhizobium and Sinorhizobium showed patterns of gene presence and absence consistent with the phylogenetic diversification of six major clades identified in the ribosomal phylogenomic tree (Supplementary Figure S1). Accordingly, we found that the number of RepC families of chromids and plasmids was small and less diverse than suggested by electrophoretic patterns of Rhizobium isolates (Figure 5) (Jumas-Bilak et al, 1998; Mazur et al, 2011; Zahran, 2017). The apparent high plasmid diversity in Rhizobium probably arose from DNA rearrangements, like replicon fusion or fissions, as well as from insertions and deletions (González et al, 2010; Pérez Carrascal et al, 2016).…”

Section: Discussionmentioning

confidence: 66%

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Phylogenomic Rhizobium Species Are Structured by a Continuum of Diversity and Genomic Clusters

et al. 2019

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The bacterial genus Rhizobium comprises diverse symbiotic nitrogen-fixing species associated with the roots of plants in the Leguminosae family. Multiple genomic clusters defined by whole genome comparisons occur within Rhizobium , but their equivalence to species is controversial. In this study we investigated such genomic clusters to ascertain their significance in a species phylogeny context. Phylogenomic inferences based on complete sets of ribosomal proteins and stringent core genome markers revealed the main lineages of Rhizobium . The clades corresponding to R. etli and R. leguminosarum species show several genomic clusters with average genomic nucleotide identities (ANI > 95%), and a continuum of divergent strains, respectively. They were found to be inversely correlated with the genetic distance estimated from concatenated ribosomal proteins. We uncovered evidence of a Rhizobium pangenome that was greatly expanded, both in its chromosomes and plasmids. Despite the variability of extra-chromosomal elements, our genomic comparisons revealed only a few chromid and plasmid families. The presence/absence profile of genes in the complete Rhizobium genomes agreed with the phylogenomic pattern of species divergence. Symbiotic genes were distributed according to the principal phylogenomic Rhizobium clades but did not resolve genome clusters within the clades. We distinguished some types of symbiotic plasmids within Rhizobium that displayed different rates of synonymous nucleotide substitutions in comparison to chromosomal genes. Symbiotic plasmids may have been repeatedly transferred horizontally between strains and species, in the process displacing and substituting pre-existing symbiotic plasmids. In summary, the results indicate that Rhizobium genomic clusters, as defined by whole genomic identities, might be part of a continuous process of evolutionary divergence that includes the core and the extrachromosomal elements leading to species formation.

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Section: Discussionmentioning

confidence: 66%

“…Horizontal transfer of pSyms has been proposed to occur repeatedly in Rhizobium evolution (Martínez-Romero, 2009; Rogel et al, 2014; Zahran, 2017). In the process, owing to displacement and substitution effects, incongruent evolution rates between the chromosome and pSym are expected.…”

Section: Resultsmentioning

confidence: 99%

Phylogenomic Rhizobium Species Are Structured by a Continuum of Diversity and Genomic Clusters

et al. 2019

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“…Increasing evidence has been mounting regarding the accessory plasmids' influence on legume‐rhizobia symbiosis under stress, such as resistance to heat, acid, antibiotics, heavy metals, pesticides and oxidative stress protection (Kurchak et al ., ; Streit et al ., , 234; Anjum et al ., ; Vercruysse et al ., ; Naamala et al ., ). Therefore, it is of significance to uncover novel characteristics and functions of different PUCs and then determine their influence on the symbiotic interactions between legumes and rhizobia, in niches with diverse and harsh environmental conditions (Zahran, ).…”

Section: Discussionmentioning

confidence: 99%

“…The plasmids in rhizobia are typically divided into two main groups: the symbiotic plasmid (pSym) carrying the symbiosis module in which genes essential for nodulation, infection, and nitrogen fixation are clustered, and the non‐symbiotic/accessory plasmids (Remigi et al ., ). Unlike the pSym encoding for symbiotic activity, the accessory plasmids enable the host rhizobia to survive in diverse habitats and under stress conditions (diCenzo et al ., ; Zahran, ). Comparatively, the accessory plasmids have gained limited attention and experimental investigations have been difficult to perform because of their high variability and ability to easily exchange genetic material between and within species (Dresler‐Nurmi et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

Wang

Tong

et al. 2019

Environmental Microbiology

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Summary The genus Rhizobium usually has a multipartite genome architecture with a chromosome and several plasmids, making these bacteria a perfect candidate for plasmid biology studies. As there are no universally shared genes among typical plasmids, network analyses can complement traditional phylogenetics in a broad‐scale study of plasmid evolution. Here, we present an exhaustive analysis of 216 plasmids from 49 complete genomes of Rhizobium by constructing a bipartite network that consists of two classes of nodes, the plasmids and homologous protein families that connect them. Dissection of the network using a hierarchical clustering strategy reveals extensive variety, with 34 homologous plasmid clusters. Four large clusters including one cluster of symbiotic plasmids and two clusters of chromids carrying some truly essential genes are widely distributed among Rhizobium. In contrast, the other clusters are quite small and rare. Symbiotic clusters and rare accessory clusters are exogenetic and do not appear to have co‐evolved with the common accessory clusters; the latter ones have a large coding potential and functional complementarity for different lifestyles in Rhizobium. The bipartite network also provides preliminary evidence of Rhizobium plasmid variation and formation including genetic exchange, plasmid fusion and fission, exogenetic plasmid transfer, host plant selection, and environmental adaptation.

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“…The N 2 -fixing symbiosis between most legumes and bacteria is a well-studied example of the formation of root nodules, and occasionally stem nodules, which are induced and subsequently invaded by specific rhizobia. Phylogenetic studies have shown that, based on a diverse range of legume species, over 150 rhizobial species belonging to 12 genera of Alphaproteobacteria and two genera of Betaprotebacteria occupied the root nodules tested (Peix et al, 2015 ; Zahran, 2017 ). In various legumes, in addition to rhizobia that are responsible for nodulation and N 2 fixation, other endophytic bacteria, called non-rhizobial bacteria, are also found in the nodules (Sachs and Simms, 2008 ; Wu et al, 2011 ; Busby et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Co-existence of Rhizobia and Diverse Non-rhizobial Bacteria in the Rhizosphere and Nodules of Dalbergia odorifera Seedlings Inoculated with Bradyrhizobium elkanii, Rhizobium multihospitium–Like and Burkholderia pyrrocinia–Like Strains

Yang

Wang

et al. 2017

Front. Microbiol.

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Rhizobia induce root nodules and fix atmospheric N2 for most legume species in exchange for carbon. However, the diverse endophytic non-rhizobial bacteria in legume nodules that co-exist with rhizobia are often ignored because they are difficult to cultivate using routine cultivation approaches. To enhance our understanding of the incidence and diversity of legume–bacteria associations, a high-throughput sequencing analysis of bacterial 16S rRNA genes was used to examine the bacterial community in the rhizospheres and root nodules of Dalbergia odorifera seedlings that were uninoculated or inoculated with Bradyrhizobium elkanii H255, Rhizobium multihospitium–like HT221, or Burkholderia pyrrocinia–like H022238, in two growth media (nitrogen [N]-supplied soil or N-omitted potting mix). Seedlings inoculated with Bradyrhizobium had significantly more nodules than seedlings in the other inoculation conditions, regardless of growth media. Using the 15N natural abundance method, it was shown that the inoculated plants had significantly higher N2 fixation efficiency (48–57%) and specific nodule activity [269–313 μg N mg−1 of dry weight (dwt) nodule] compared to the uninoculated plants (203 μg N mg−1 dwt nodule). The 16S rRNA gene analysis showed that there was generally a higher bacterial diversity in the rhizosphere than in the nodules in the corresponding condition. Both rhizobial inoculation and media status significantly altered the bacterial communities in the rhizospheres and nodules (P < 0.05), with the exception of the inoculated soil rhizospheres. Regarding non-rhizobial bacteria, three genera, i.e., Lactococcus, Bacillus, and Pseudomonas, were consistently enriched in the rhizosphere and Bradyrhizobium, Chloroplast norank (which belongs to Cyanobacteria), and Lactococcus were commonly found in the nodules. In contrast, common rhizobial genera (including Rhizobium, Mesorhizobium, and Burkholderia) were only present in the nodules at low relative abundances (0.01–3.41%). Regarding non-rhizobial bacteria, 32 genera were found in the nodules, with non-rhizobial bacteria being predominant in the N omitted potting mix (with a relative abundance of 56–87%). This study suggests that legume nodules are inhabited by a high diversity of non-rhizobial bacteria, which may play a vital role in nodulation and N2 fixation in the host plants.

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Plasmids impact on rhizobia-legumes symbiosis in diverse environments

Cited by 15 publications

References 226 publications

Phylogenomic Rhizobium Species Are Structured by a Continuum of Diversity and Genomic Clusters

Phylogenomic Rhizobium Species Are Structured by a Continuum of Diversity and Genomic Clusters

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

Co-existence of Rhizobia and Diverse Non-rhizobial Bacteria in the Rhizosphere and Nodules of Dalbergia odorifera Seedlings Inoculated with Bradyrhizobium elkanii, Rhizobium multihospitium–Like and Burkholderia pyrrocinia–Like Strains

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