1887

Abstract

The Gram-positive genus is currently divided into seven species (, , , , , and ) and three subspecies ( subsp. , subsp. and subsp. ). Recent studies have indicated that the taxonomic rank of the subspecies must be re-evaluated. In this research, we assessed the taxonomic position of the three subspecies and clarified the taxonomic nomenclature of other 75 strains. The complete genomes of the type strains of the three subspecies, the type strain of and A6096 were sequenced using PacBio RSII technology. Application of whole-genome-based computational approaches such as average nucleotide identity (ANI), digital DNA–DNA hybridization, multi-locus sequence analysis of seven housekeeping genes (, , , , , and ), a phylogenomic tree reconstructed from 1 028 core genes, and ANI-based phylogeny provided sufficient justification for raising subsp. to the species level. These results led us to propose the establishment of sp. nov. as a species with its type strain C55 (=CFBP 8216=ATCC BAA-2691). Moreover, the orthologous and dot plot analyses, along with the above described bioinformatic strategies, revealed a high degree of similarity between subsp. and subsp. . Based on these analyses, we propose that both subspecies be combined into a single taxon and elevated to the species level as sp. nov., with LPPA 982 (= CECT 8144= LMG 27667) as the type strain.

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2022-09-15
2024-05-02
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References

  1. Davis MJ, Gillaspie AG, Vidaver AK, Harris RW. Clavibacter: a new genus containing some phytopathogenic coryneform bacteria, including Clavibacter xyli subsp. xyli sp. nov., subsp. nov. and Clavibacter xyli subsp. cynodontis subsp. nov., pathogens that cause ratoon stunting disease of sugarcane and Bermudagrass stunting disease. Int J Syst Bacteriol 1984; 34:107–117 [View Article]
    [Google Scholar]
  2. Eichenlaub R, Gartemann K-H. The Clavibacter michiganensis subspecies: molecular investigation of Gram-positive bacterial plant pathogens. Annu Rev Phytopathol 2011; 49:445–464 [View Article] [PubMed]
    [Google Scholar]
  3. Eichenlaub R, Gartemann K-H, Burger A. Clavibacter michiganensis, a group of Gram-positive phytopathogenic bacteria. In Plant-Associated Bacteria The Netherlands: Springer, Dordrecht; 2006 pp 385–421
    [Google Scholar]
  4. de León L, Siverio F, López MM, Rodríguez A. Clavibacter michiganesis subsp. michiganensis, a seedborne tomato pathogen: healthy seeds are still the goal. Plant Dis 2011; 95:1328–1338 [View Article] [PubMed]
    [Google Scholar]
  5. Lu Y, Ishimaru CA, Glazebrook J, Samac DA. Comparative genomic analyses of Clavibacter michiganensis subsp. insidiosus and pathogenicity on Medicago truncatula. Phytopathology 2018; 108:172–185 [View Article] [PubMed]
    [Google Scholar]
  6. Carlson RR, Vidaver AK. Taxonomy of Corynebacterium plant pathogens, including a new pathogen of wheat, based on polyacrylamide gel electrophoresis of cellular proteins. Int J Syst Bacteriol 1982; 32:315–326 [View Article]
    [Google Scholar]
  7. Vidaver AK, Mandel M. Corynebacterium nebraskense, a new, orange-pigmented phytopathogenic species. Int J Syst Bacteriol 1974; 24:482–485 [View Article]
    [Google Scholar]
  8. Oh E-J, Bae C, Lee H-B, Hwang IS, Lee H-I et al. Clavibacter michiganensis subsp. capsici subsp. nov., causing bacterial canker disease in pepper. Int J Syst Evol Microbiol 2016; 66:4065–4070 [View Article] [PubMed]
    [Google Scholar]
  9. González AJ, Trapiello E. Clavibacter michiganensis subsp. phaseoli subsp. nov., pathogenic in bean. Int J Syst Evol Microbiol 2014; 64:1752–1755 [View Article] [PubMed]
    [Google Scholar]
  10. European and Mediterranean Plant Protection Organization Pm 1/2 (30) EPPO A1 and A2 Lists of pests recommended for regulation as quarantine pests. Paris, France: 2021 https://gd.eppo.int/taxon/CORBIN/documents
  11. Yasuhara-Bell J, Alvarez AM. Seed-associated subspecies of the genus Clavibacter are clearly distinguishable from Clavibacter michiganensis subsp. michiganensis. Int J Syst Evol Microbiol 2015; 65:811–826 [View Article] [PubMed]
    [Google Scholar]
  12. Li X, Tambong J, Yuan KX, Chen W, Xu H et al. Re-classification of Clavibacter michiganensis subspecies on the basis of whole-genome and multi-locus sequence analyses. Int J Syst Evol Microbiol 2018; 68:234–240 [View Article] [PubMed]
    [Google Scholar]
  13. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2018; 9:2007 [View Article] [PubMed]
    [Google Scholar]
  14. Tian Q, Chuan J, Sun X, Zhou A, Wang L et al. Description of Clavibacter zhangzhiyongii sp. nov., a phytopathogenic actinobacterium isolated from barley seeds, causing leaf brown spot and decline. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
    [Google Scholar]
  15. Hugenholtz P, Chuvochina M, Oren A, Parks DH, Soo RM. Prokaryotic taxonomy and nomenclature in the age of big sequence data. ISME J 2021; 15:1879–1892 [View Article] [PubMed]
    [Google Scholar]
  16. Kämpfer P, Glaeser SP. Prokaryotic taxonomy in the sequencing era - the polyphasic approach revisited: prokaryotic taxonomy in the sequencing era. Environ Microbiol 2012; 14:291–317
    [Google Scholar]
  17. Chung M, Munro JB, Tettelin H, Dunning Hotopp JC. Using core genome alignments to assign bacterial species. mSystems 2018; 3:21 [View Article] [PubMed]
    [Google Scholar]
  18. Ciufo S, Kannan S, Sharma S, Badretdin A, Clark K et al. Using average nucleotide identity to improve taxonomic assignments in prokaryotic genomes at the NCBI. Int J Syst Evol Microbiol 2018; 68:2386–2392 [View Article] [PubMed]
    [Google Scholar]
  19. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. PNAS 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  20. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
    [Google Scholar]
  21. Auch AF, von Jan M, Klenk H-P, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article] [PubMed]
    [Google Scholar]
  22. Osdaghi E, Portier P, Briand M, Taghouti G, Jacques M-A. Draft genome sequences of the type strains of three Clavibacter subspecies and atypical peach-colored strains isolated from tomato. Microbiol Resour Announc 2018; 7:e01357-18 [View Article] [PubMed]
    [Google Scholar]
  23. Osdaghi E, Rahimi T, Taghavi SM, Ansari M, Zarei S et al. Comparative genomics and phylogenetic analyses suggest several novel species within the genus Clavibacter, including nonpathogenic tomato-associated strains. Appl Environ Microbiol 2020; 86:e02873-19 [View Article] [PubMed]
    [Google Scholar]
  24. Méndez V, Valenzuela M, Salvà-Serra F, Jaén-Luchoro D, Besoain X et al. Comparative genomics of pathogenic Clavibacter michiganensis subsp. michiganensis strains from chile reveals potential virulence features for tomato plants. Microorganisms 2020; 8:1679 [View Article] [PubMed]
    [Google Scholar]
  25. Thapa SP, Pattathil S, Hahn MG, Jacques M-A, Gilbertson RL et al. Genomic analysis of Clavibacter michiganensis reveals insight into virulence strategies and genetic diversity of a gram-positive bacterial pathogen. Mol Plant Microbe Interact 2017; 30:786–802 [View Article] [PubMed]
    [Google Scholar]
  26. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article]
    [Google Scholar]
  27. Huntemann M, Ivanova NN, Mavromatis K, Tripp HJ, Paez-Espino D et al. The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4). Stand Genomic Sci 2015; 10:86 [View Article]
    [Google Scholar]
  28. Chen I-MA, Chu K, Palaniappan K, Pillay M, Ratner A et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res 2019; 47:D666–D677 [View Article] [PubMed]
    [Google Scholar]
  29. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article]
    [Google Scholar]
  30. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005; 102:2567–2572 [View Article] [PubMed]
    [Google Scholar]
  31. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  32. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
    [Google Scholar]
  33. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  34. Parker CT, Tindall BJ, Garrity GM. International Code of Nomenclature of Prokaryotes: prokaryotic code (2008 revision). Int J Syst Evol Microbiol 2019; 69:S1–S111 [View Article]
    [Google Scholar]
  35. Załuga J, Stragier P, Baeyen S, Haegeman A, Van Vaerenbergh J et al. Comparative genome analysis of pathogenic and non-pathogenic Clavibacter strains reveals adaptations to their lifestyle. BMC Genomics 2014; 15:392 [View Article] [PubMed]
    [Google Scholar]
  36. Zaluga J, Van Vaerenbergh J, Stragier P, Maes M, De Vos P. Genetic diversity of non-pathogenic Clavibacter strains isolated from tomato seeds. Syst Appl Microbiol 2013; 36:426–435 [View Article] [PubMed]
    [Google Scholar]
  37. Jacques M-A, Durand K, Orgeur G, Balidas S, Fricot C et al. Phylogenetic analysis and polyphasic characterization of Clavibacter michiganensis strains isolated from tomato seeds reveal that nonpathogenic strains are distinct from C. michiganensis subsp. michiganensis. Appl Environ Microbiol 2012; 78:8388–8402 [View Article]
    [Google Scholar]
  38. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  39. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article]
    [Google Scholar]
  40. Löytynoja A. Phylogeny-aware alignment with PRANK. In Russell DJ. eds Multiple Sequence Alignment Methods Totowa, NJ: Humana Press; 2014 pp 155–170 [View Article]
    [Google Scholar]
  41. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
    [Google Scholar]
  42. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  43. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178–2189 [View Article] [PubMed]
    [Google Scholar]
  44. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R et al. Circos: an information aesthetic for comparative genomics. Genome Res 2009; 19:1639–1645 [View Article] [PubMed]
    [Google Scholar]
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