1887

Abstract

In 2015, Gram-positive peach-coloured actinobacterial strains were isolated from symptomless tomato phyllosphere in Iran. Biochemical and physiological characteristics, as well as 16S rRNA phylogeny showed that the strains belong to sp., while they were non-pathogenic on the host of isolation, and morphologically distinct from the tomato pathogen and other plant-associated bacteria. Multilocus sequence analysis of five housekeeping genes showed that the two peach-coloured strains CFBP 8615 (Tom532) and CFBP 8616 (Tom495) were phylogenetically distinct from all validly described species. Whole genome sequence-based indices, i.e. average nucleotide identity (orthoANI) and digital DNA-DNA hybridization (dDDH), showed that the two peach-colored strains share nearly 100 % orthoANI value with one another, while they differ from all validly described species with the orthoANI/dDDH values <93 % and <50 %, respectively. Thus, based on both phenotypic features and orthoANI/dDDH indices the peach-coloured strains could belong to a new species within . In this study, we provide a formal species description for the peach-coloured tomato-associated strains. sp. nov. is proposed for the new species with Tom532 = CFBP 8615 = ICMP 22100 as type strain.

Funding
This study was supported by the:
  • Iran National Science Foundation (Award 4015022)
    • Principle Award Recipient: EbrahimOsdaghi
  • College of Agriculture Natural Resources, University of Tehran
    • Principle Award Recipient: EbrahimOsdaghi
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006022
2023-09-21
2024-05-08
Loading full text...

Full text loading...

References

  1. Ansari M, Taghavi SM, Hamzehzarghani H, Valenzuela M, Siri MI et al. Multiple introductions of tomato pathogen Clavibacter michiganensis subsp. michiganensis into Iran as revealed by a global-scale phylogeographic analysis. Appl Environ Microbiol 2019; 85:e02098-19 [View Article] [PubMed]
    [Google Scholar]
  2. Dye DW, Kemp WJ. A taxonomic study of plant pathogenic Corynebacterium species. New Zeal J Agr Res 1977; 20:563–582 [View Article]
    [Google Scholar]
  3. 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] [PubMed]
    [Google Scholar]
  4. EPPO PM 1/2 (31) EPPO A1 and A2 lists of pests recommended for regulation as quarantine pests; 2022
  5. Osdaghi E, van der Wolf JM, Abachi H, Li X, De Boer SH et al. Bacterial ring rot of potato caused by Clavibacter sepedonicus: a successful example of defeating the enemy under international regulations. Mol Plant Pathol 2022; 23:911–932 [View Article] [PubMed]
    [Google Scholar]
  6. CABI Clavibacter michiganensis (bacterial canker of tomato). Invasive Species Compendium. Wallingford, UK: CABI; 2022 https://www.cabi.org/isc/datasheet/15338
  7. Davis MJ, Gillaspie AG, JrVidaver 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 1984107–117 [View Article]
    [Google Scholar]
  8. Davis MJ, Vidaver AK. Coryneform plant pathogens. In Schaad NW, Jones JB, Chun W. eds Laboratory Guide for Identification of Plant Ppathogenic Bacteria, 3rd. edn USA; 2001
    [Google Scholar]
  9. 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]
  10. EPPO PM 7/42 (3) Clavibacter michiganensis subsp. michiganensis. EPPO Bull 2016; 46:202–225 [View Article]
    [Google Scholar]
  11. Osdaghi E, Robertson AE, Jackson-Ziems TA, Abachi H, Li X et al. Clavibacter nebraskensis causing Goss’s wilt of maize: five decades of detaining the enemy in the New World. Mol Plant Pathol 2022; 24:675–692 [View Article] [PubMed]
    [Google Scholar]
  12. 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]
  13. 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]
  14. 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]
  15. 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]
  16. 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]
  17. 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; 71:004786 [View Article] [PubMed]
    [Google Scholar]
  18. Arizala D, Dobhal S, Alvarez AM, Arif M. Elevation of Clavibacter michiganensis subsp. californiensis to species level as Clavibacter californiensis sp. nov., merging and re-classification of Clavibacter michiganensis subsp. chilensis and Clavibacter michiganensis subsp. phaseoli as Clavibacter phaseoli sp. nov. based on complete genome in silico analyses. Int J Syst Evol Microbiol 2022; 72: [View Article]
    [Google Scholar]
  19. Osdaghi E, Ansari M, Taghavi SM, Zarei S, Koebnik R et al. Pathogenicity and phylogenetic analysis of Clavibacter michiganensis strains associated with tomato plants in Iran. Plant Pathol 2018; 67:957–970 [View Article]
    [Google Scholar]
  20. Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Harveson RM et al. Epiphytic Curtobacterium flaccumfaciens strains isolated from symptomless solanaceous vegetables are pathogenic on leguminous but not on solanaceous plants. Plant Pathol 2018; 67:388–398 [View Article]
    [Google Scholar]
  21. Koblitz J, Halama P, Spring S, Thiel V, Baschien C et al. MediaDive: the expert-curated cultivation media database. Nucleic Acids Res 2023; 51:D1531–D1538 [View Article] [PubMed]
    [Google Scholar]
  22. Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Harveson RM et al. Occurrence and characterization of a new red-pigmented variant of Curtobacterium flaccumfaciens, the causal agent of bacterial wilt of edible dry beans in Iran. Eur J Plant Pathol 2016; 146:129–145 [View Article]
    [Google Scholar]
  23. Schaad NW, Jones JB, Chun W. Laboratory guide for the identification of plant pathogenic bacteria, 3rd. edn American Phytopathological Society (APS Press); 2001
    [Google Scholar]
  24. Osdaghi E, Taghavi SM, Calamai S, Biancalani C, Cerboneschi M et al. Phenotypic and molecular-phylogenetic analysis provide novel insights into the diversity of Curtobacterium flaccumfaciens. Phytopathology 2018; 108:1154–1164 [View Article] [PubMed]
    [Google Scholar]
  25. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  26. Osdaghi E, Taghouti G, Dutrieux C, Taghavi SM, Fazliarab A et al. Whole genome resources of 17 Curtobacterium flaccumfaciens strains including pathotypes of C. flaccumfaciens pv. betae, C. flaccumfaciens pv. oortii and C. flaccumfaciens pv. poinsettiae.. Mol Plant Microbe Interact 2022; 35:352–356 [View Article]
    [Google Scholar]
  27. Luo R, Liu B, Xie Y, Li Z, Huang W et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 2012; 1:18 [View Article] [PubMed]
    [Google Scholar]
  28. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article] [PubMed]
    [Google Scholar]
  29. Borodovsky M, Lomsadze A. Gene identification in prokaryotic genomes, phages, metagenomes, and EST sequences with GeneMarkS suite. Curr Protoc Microbiol 2014; 32:Unit 1E.7 [View Article] [PubMed]
    [Google Scholar]
  30. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
    [Google Scholar]
  31. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  32. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ 2016 [View Article]
    [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. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  35. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  36. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article] [PubMed]
    [Google Scholar]
  37. Kotchoni SO, Gachomo EW, Betiku E, Shonukan OO. A home made kit for Plasmid DNA mini-preparation. Afr J Biotechnol 2003; 2:88–90
    [Google Scholar]
  38. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article] [PubMed]
    [Google Scholar]
  39. Chen G, Khojasteh M, Taheri-Dehkordi A, Taghavi SM, Rahimi T et al. Complete genome sequencing provides novel insight into the virulence repertories and phylogenetic position of dry beans pathogen Curtobacterium flaccumfaciens pv. flaccumfaciens. Phytopathology 2021; 111:268–280 [View Article] [PubMed]
    [Google Scholar]
  40. Osdaghi E, Young AJ, Harveson RM. Bacterial wilt of dry beans caused by Curtobacterium flaccumfaciens pv. flaccumfaciens: a new threat from an old enemy. Mol Plant Pathol 2020; 21:605–621 [View Article] [PubMed]
    [Google Scholar]
  41. Haghverdi Determining the sources of Clavibacter michiganensis subsp. michiganensis, the causative agent of tomato bacterial canker disease and the response of different tomato cultivars to the disease MSc thesis, Shiraz University; 2021
    [Google Scholar]
  42. Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Lamichhane JR. Monitoring the occurrence of tomato bacterial spot and range of the causal agent Xanthomonas perforans in Iran. Plant Pathol 2017; 66:990–1002 [View Article]
    [Google Scholar]
  43. Osdaghi E, Taghavi SM, Hamzehzarghani H, Lamichhane JR. Occurrence and characterization of the bacterial spot pathogen Xanthomonas euvesicatoria on pepper in Iran. J Phytopathol 2016; 164:722–734 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006022
Loading
/content/journal/ijsem/10.1099/ijsem.0.006022
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error