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Genomic analysis provides novel insights into diversification and taxonomy of Allorhizobium vitis (i.e. Agrobacterium vitis)

View ORCID ProfileNemanja Kuzmanović, Enrico Biondi, Jörg Overmann, Joanna Puławska, Susanne Verbarg, Kornelia Smalla, View ORCID ProfileFlorent Lassalle
doi: https://doi.org/10.1101/2020.12.19.423612
Nemanja Kuzmanović
1Julius Kühn Institute, Federal Research Centre for Cultivated Plants (JKI), Institute for Epidemiology and Pathogen Diagnostics, Messeweg 11-12, 38104 Braunschweig, Germany
2Julius Kühn Institute, Federal Research Centre for Cultivated Plants (JKI), Institute for Plant Protection in Horticulture and Forests, Messeweg 11-12, 38104 Braunschweig, Germany
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  • ORCID record for Nemanja Kuzmanović
  • For correspondence: kuzmanovic1306@gmail.com nemanja.kuzmanovic@julius-kuehn.de f.lassalle@imperial.ac.uk
Enrico Biondi
3Alma Mater Studiorum - University of Bologna, Viale G. Fanin, 42, 40127 Bologna, Italy
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Jörg Overmann
4Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Inhoffenstrasse 7B, 38124 Braunschweig, Germany
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Joanna Puławska
5Research Institute of Horticulture, ul. Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland
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Susanne Verbarg
4Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Inhoffenstrasse 7B, 38124 Braunschweig, Germany
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Kornelia Smalla
1Julius Kühn Institute, Federal Research Centre for Cultivated Plants (JKI), Institute for Epidemiology and Pathogen Diagnostics, Messeweg 11-12, 38104 Braunschweig, Germany
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Florent Lassalle
6Imperial College London, St-Mary’s Hospital campus, Department of Infectious Disease Epidemiology, Praed Street, London W2 1NY, UK; Imperial College London, St-Mary’s Hospital campus, MRC Centre for Global Infectious Disease Analysis, Praed Street, London W2 1NY, United Kingdom
7Wellcome Sanger Institute, Pathogens and Microbes Programme, Wellcome Genome Campus, Hinxton, Saffron Walden, CB10 1RQ, United Kingdom
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  • ORCID record for Florent Lassalle
  • For correspondence: kuzmanovic1306@gmail.com nemanja.kuzmanovic@julius-kuehn.de f.lassalle@imperial.ac.uk
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Abstract

Background Allorhizobium vitis (formerly named Agrobacterium vitis or Agrobacterium biovar 3) is the primary causative agent of crown gall disease of grapevine worldwide. We obtained and analyzed whole-genome sequences of diverse All. vitis strains to get insights into their diversification and taxonomy.

Results Pairwise genome comparisons and phylogenomic analysis of various All. vitis strains clearly indicated that All. vitis is not a single species, but represents a species complex composed of several genomic species. Thus, we emended the description of All. vitis, which now refers to a restricted group of strains within the All. vitis species complex (i.e. All. vitis sensu stricto) and proposed a description of a novel species, All. ampelinum sp. nov. The type strain of All. vitis sensu stricto remains the current type strain of All. vitis, K309T. The type strain of All. ampelinum sp. nov. is S4T. We also identified sets of gene clusters specific to the All. vitis species complex, All. vitis sensu stricto and All. ampelinum, respectively, for which we predicted the biological function and infer the role in ecological diversification of these clades, including some we could experimentally validate. All. vitis species complex-specific genes confer tolerance to different stresses, including exposure to aromatic compounds. Similarly, All. vitis sensu stricto-specific genes confer the ability to degrade 4-hydroxyphenylacetate and a putative compound related to gentisic acid. All. ampelinum-specific genes have putative functions related to polyamine metabolism and nickel assimilation. Congruently with the genome-based classification, All. vitis sensu stricto and All. ampelinum were clearly delineated by MALDI-TOF MS analysis. Moreover, our genome-based analysis indicated that Allorhizobium is clearly separated from other genera of the family Rhizobiaceae.

Conclusions Comparative genomics and phylogenomic analysis provided novel insights into the diversification and taxonomy of Allorhizobium vitis species complex, supporting our redefinition of All. vitis sensu stricto and description of All. ampelinum. Our pan-genome analyses suggest that these species have differentiated ecologies, each relying on specialized nutrient consumption or toxic compound degradation to adapt to their respective niche.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Title change; Abstract modified; Results section updated; Supplemental files updated;

  • https://figshare.com/projects/Allorhizobium_vitis/125029

  • Abbreviations

    AAI
    Average amino acid identity
    AF
    Alignment fraction
    ANI
    Average nucleotide identity
    DDH
    DNA-DNA hybridization
    dDDH
    Digital DDH
    gANI
    Genome-wide ANI
    MS
    Mass-spectrometry
    OGRI
    Overall genome relatedness index
    MLSA
    Multi-locus sequence analysis
    PGAP
    Prokaryotic genomes annotation pipeline
    POCP
    Percentage of conserved proteins
    TAR
    Tartrate utilization
    Ti
    Tumor-inducing
  • Copyright 
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    Posted December 05, 2021.
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    Genomic analysis provides novel insights into diversification and taxonomy of Allorhizobium vitis (i.e. Agrobacterium vitis)
    Nemanja Kuzmanović, Enrico Biondi, Jörg Overmann, Joanna Puławska, Susanne Verbarg, Kornelia Smalla, Florent Lassalle
    bioRxiv 2020.12.19.423612; doi: https://doi.org/10.1101/2020.12.19.423612
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    Genomic analysis provides novel insights into diversification and taxonomy of Allorhizobium vitis (i.e. Agrobacterium vitis)
    Nemanja Kuzmanović, Enrico Biondi, Jörg Overmann, Joanna Puławska, Susanne Verbarg, Kornelia Smalla, Florent Lassalle
    bioRxiv 2020.12.19.423612; doi: https://doi.org/10.1101/2020.12.19.423612

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