Divergent Evolution of Symbiotic Bacteria: Rhizobia of the Relic Legume Vavilovia formosa Form an Isolated Group within Rhizobium leguminosarum bv. viciae

Kimeklis, Anastasiia K.; Kuznetsova, I. G.; Sazanova, Anna L; Safronova, Vera I.; Belimov, Andrey A.; Онищук, О. П.; Курчак, О. Н.; Аксенова, Т. С.; Пинаев, А. Г.; Мусаев, А. М.; Andronov, E. E.; Проворов, Н. А.

doi:10.1134/s1022795418070062

Cited by 5 publications

(4 citation statements)

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“…In order to analyse the trade-off between symbiotic diversification and speciation processes in rhizobia, we compared the divergence of hkg and sym genes. Previously, we demonstrated that the Vaf group diverged from the Rlv and Rlt groups for sym genes, but not for hkg genes [45]. In this report, with the help of group separation statistics, we demonstrated that intergroup divergence pertains to both gene categories ( Figure 5), although in hkg genes it is not pronounced enough to result in the emergence of new species.…”

Section: Divergent Evolution Within R Leguminosarumsupporting

confidence: 50%

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Rhizobia Isolated from the Relict Legume Vavilovia formosa Represent a Genetically Specific Group within Rhizobium leguminosarum biovar viciae

Kimeklis

Chirak

Kuznetsova

et al. 2019

Genes

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Twenty-two rhizobia strains isolated from three distinct populations (North Ossetia, Dagestan, and Armenia) of a relict legume Vavilovia formosa were analysed to determine their position within Rhizobium leguminosarum biovar viciae (Rlv). These bacteria are described as symbionts of four plant genera Pisum, Vicia, Lathyrus, and Lens from the Fabeae tribe, of which Vavilovia is considered to be closest to its last common ancestor (LCA). In contrast to biovar viciae, bacteria from Rhizobium leguminosarum biovar trifolii (Rlt) inoculate plants from the Trifolieae tribe. Comparison of house-keeping (hkg: 16S rRNA, glnII, gltA, and dnaK) and symbiotic (sym: nodA, nodC, nodD, and nif H) genes of the symbionts of V. formosa with those of other Rlv and Rlt strains reveals a significant group separation, which was most pronounced for sym genes. A remarkable feature of the strains isolated from V. formosa was the presence of the nodX gene, which was commonly found in Rlv strains isolated from Afghanistan pea genotypes. Tube testing of different strains on nine plant species, including all genera from the Fabeae tribe, demonstrated that the strains from V. formosa nodulated the same cross inoculation group as the other Rlv strains. Comparison of nucleotide similarity in sym genes suggested that their diversification within sym-biotypes of Rlv was elicited by host plants. Contrariwise, that of hkg genes could be caused by either local adaptation to soil niches or by genetic drift. Long-term ecological isolation, genetic separation, and the ancestral position of V. formosa suggested that symbionts of V. formosa could be responsible for preserving ancestral genotypes of the Rlv biovar. may be traced using specialised symbiotic (sym) genes representing the accessory parts of bacterial genomes, which differ in their natural histories from housekeeping genes (hkg) representing the core parts of genomes [4]. As a result of co-evolutionary processes, symbiosis is formed between tightly co-adapted cross-inoculation groups of rhizobia and legumes, and their coevolution is directed by a set of symbiosis-specific genes from each partner [5][6][7]. In some rhizobia, sym genes are more susceptible to autonomous horizontal gene transfer than hkg genes, because they are located on plasmids-mobile elements of the genome [3]. This results in an intensive recombination of host specific and chromosomal markers [8]. For example, Rhizobium leguminosarum is composed of two biovars, which have diverged based on their plasmid-encoded host ranges [9]. Biovar viciae (Rlv) nodulates legumes from the Fabeae tribe, while biovar trifolii (Rlt) nodulates clovers from the Trifolieae tribe; however, they show a conservative chromosomal arrangement of hkg markers (Figure 1).Even so, divergent evolution of rhizobia is not restricted to sym genes. Application of the average nucleotide identity (ANI) method has demonstrated that a local R. leguminosarum population could be separated into five genomic species, differing in their hkg genes, representing their cor...

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Section: Divergent Evolution Within R Leguminosarumsupporting

confidence: 50%

“…We also demonstrated that the V. formosa isolates differed from other bv. viciae strains in their sym gene sequences; however, they did not differ in their hkg sequences [45].…”

Section: Discussionmentioning

confidence: 79%

Rhizobia Isolated from the Relict Legume Vavilovia formosa Represent a Genetically Specific Group within Rhizobium leguminosarum biovar viciae

Kimeklis

Chirak

Kuznetsova

et al. 2019

Genes

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“…viciae required to probe this hypothesis represented the priorities of our research. Previously, Kimeklis et al [19,22] showed that at the gene level (especially in sym genes) rhizobia isolated from Vavilovia nodules represent a well-defined group within R. leguminosarum bv. viciae, which is genetically different from the strains isolated from Pisum and Vicia species.…”

Section: Introductionmentioning

confidence: 99%

Search for Ancestral Features in Genomes of Rhizobium leguminosarum bv. viciae Strains Isolated from the Relict Legume Vavilovia formosa

Chirak

Kimeklis

Karasev

et al. 2019

Genes

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Vavilovia formosa is a relict leguminous plant growing in hard-to-reach habitats in the rocky highlands of the Caucasus and Middle East, and it is considered as the putative closest living relative of the last common ancestor (LCA) of the Fabeae tribe. Symbionts of Vavilovia belonging to Rhizobium leguminosarum bv. viciae compose a discrete group that differs from the other strains, especially in the nucleotide sequences of the symbiotically specialised (sym) genes. Comparison of the genomes of Vavilovia strains with the reference group composed of R. leguminosarum bv. viciae strains isolated from Pisum and Vicia demonstrated that the vavilovia strains have a set of genomic features, probably indicating the important stages of microevolution of the symbiotic system. Specifically, symbionts of Vavilovia (considered as an ancestral group) demonstrated a scattered arrangement of sym genes (>90 kb cluster on pSym), with the location of nodT gene outside of the other nod operons, the presence of nodX and fixW, and the absence of chromosomal fixNOPQ copies. In contrast, the reference (derived) group harboured sym genes as a compact cluster (<60 kb) on a single pSym, lacking nodX and fixW, with nodT between nodN and nodO, and possessing chromosomal fixNOPQ copies. The TOM strain, obtained from nodules of the primitive "Afghan" peas, occupied an intermediate position because it has the chromosomal fixNOPQ copy, while the other features, the most important of which is presence of nodX and fixW, were similar to the Vavilovia strains. We suggest that genome evolution from the ancestral to the derived R. leguminosarum bv. viciae groups follows the "gain-and-loss of sym genes" and the "compaction of sym cluster" strategies, which are common for the macro-evolutionary and micro-evolutionary processes. The revealed genomic features are in concordance with a relict status of the vavilovia strains, indicating that V. formosa coexists with ancestral microsymbionts, which are presumably close to the LCA of R. leguminosarum bv. viciae.

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“…Suitable models to address the trade-off between intra-species diversification and speciation are represented by fast-growing rhizobia from the Rhizobiaceae family characterized by narrow host ranges towards the Galegoid legumes ( Figure 2 ). We demonstrated ( Kimeklis et al., 2018 ; Kimeklis et al., 2019 ) that in Rhizobium leguminosarum , the symbiotically contrasting biovars viciae (associated with the legume tribe Fabeae) and trifolii (associated with clovers from the Trifolieae tribe) are either not diverged for hkg s (p-distance analysis) or their divergence is sufficiently lower than for sym genes (group separation analysis).…”

Section: Microevolution and Speciation: Divergence Of Rhizobia Genomesmentioning

confidence: 88%

Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns

Проворов¹,

Andronov²,

Kimeklis³

et al. 2022

Front. Plant Sci.

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Nodule bacteria (rhizobia), N2-fixing symbionts of leguminous plants, represent an excellent model to study the fundamental issues of evolutionary biology, including the tradeoff between microevolution, speciation, and macroevolution, which remains poorly understood for free-living organisms. Taxonomically, rhizobia are extremely diverse: they are represented by nearly a dozen families of α-proteobacteria (Rhizobiales) and by some β-proteobacteria. Their genomes are composed of core parts, including house-keeping genes (hkg), and of accessory parts, including symbiotically specialized (sym) genes. In multipartite genomes of evolutionary advanced fast-growing species (Rhizobiaceae), sym genes are clustered on extra-chromosomal replicons (megaplasmids, chromids), facilitating gene transfer in plant-associated microbial communities. In this review, we demonstrate that in rhizobia, microevolution and speciation involve different genomic and ecological mechanisms: the first one is based on the diversification of sym genes occurring under the impacts of host-induced natural selection (including its disruptive, frequency-dependent and group forms); the second one—on the diversification of hkgs under the impacts of unknown factors. By contrast, macroevolution represents the polyphyletic origin of super-species taxa, which are dependent on the transfer of sym genes from rhizobia to various soil-borne bacteria. Since the expression of newly acquired sym genes on foreign genomic backgrounds is usually restricted, conversion of resulted recombinants into the novel rhizobia species involves post-transfer genetic changes. They are presumably supported by host-induced selective processes resulting in the sequential derepression of nod genes responsible for nodulation and of nif/fix genes responsible for symbiotic N2 fixation.

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Divergent Evolution of Symbiotic Bacteria: Rhizobia of the Relic Legume Vavilovia formosa Form an Isolated Group within Rhizobium leguminosarum bv. viciae

Cited by 5 publications

References 10 publications

Rhizobia Isolated from the Relict Legume Vavilovia formosa Represent a Genetically Specific Group within Rhizobium leguminosarum biovar viciae

Rhizobia Isolated from the Relict Legume Vavilovia formosa Represent a Genetically Specific Group within Rhizobium leguminosarum biovar viciae

Search for Ancestral Features in Genomes of Rhizobium leguminosarum bv. viciae Strains Isolated from the Relict Legume Vavilovia formosa

Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns

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