Proposal for the creation of a new genus gen. nov., reclassification of (Samson . 2005) as comb. nov. and description of a new species sp. nov. No Access

Abstract

The family of important plant pathogens includes the genus . There are currently 12 described species of , although some are poorly characterized at the genomic level. Only two genomes of , the type strain CFBP 4178 and strain Ech703, have previously been sequenced. Members of this species are mostly of tropical or subtropical origin. During an investigation of strains present in our laboratory collection we sequenced the atypical strain A3967, registered as CFBP 722, isolated from (tomato) in the South of France in 1965. The genome of strain A3967 shares digital DNA–DNA hybridization and average nucleotide identity (ANI) values of 68 and 96 %, respectively, with the type strain CFBP 4178. However, ANI analysis showed that strains are significantly dissimilar to the other species, such that less than one third of their genomes align to any other genome. On phenotypic, phylogenetic and genomic grounds, we propose a reassignment of to the genus level, for which we propose the name gen. nov., with as the type species and CFBP 4178 (NCPPB 2511) as the type strain. Phenotypic analysis showed differences between strain A3967 and CFBP 4178, such as for the assimilation of melibiose, raffinose and -inositol. These results support the description of two novel species, namely comb. nov. and sp. nov., with CFBP 4178 (NCPPB 2511=LMG 2542) and A3967 (CFBP 8732=LMG 31880) as the type strains, respectively.

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2021-10-07
2024-03-29
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References

  1. Charkowski A, Blanco C, Condemine G, Expert D, Franza T et al. The role of secretion systems and small molecules in soft-rot Enterobacteriaceae pathogenicity. Annu Rev Phytopathol 2012; 50:425–449 [View Article] [PubMed]
    [Google Scholar]
  2. Hugouvieux-Cotte-Pattat N, Condemine G, Gueguen E, Shevchik VE. Dickeya plant pathogens. eLS 2020 [View Article]
    [Google Scholar]
  3. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 2012; 13:614–629 [View Article] [PubMed]
    [Google Scholar]
  4. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the “Enterobacteriales”: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66:5575–5599 [View Article] [PubMed]
    [Google Scholar]
  5. Winslow CE, Broadhurst J, Buchanan RE, Krumwiede C, Rogers LA et al. The families and genera of the bacteria. Final report of the Committee of the Society of American Bacteriologists on characterization and classification of bacterial types. J Bacteriol 1920; 5:191–229 [View Article] [PubMed]
    [Google Scholar]
  6. Young JM, Dye DW, Bradbury JF, Panagopoulos CG, Robbs CF. A proposed nomenclature and classification for plant pathogenic bacteria. NZ J Agric Res 2012; 21:153–177 [View Article]
    [Google Scholar]
  7. Lelliott RA, Dickey RS, Genus VII. eds Erwinia. In Bergey’s Manual of Systematic Bacteriology Williams & Wilkins, Baltimore: 1984 pp 469–476
    [Google Scholar]
  8. Victoria J, Barros O. Etiologia de una neuva enfermdad bacterial del platano (Musa paradisiaca L.) en Colombia. Inst Colomb Agropecu Revista ICA 1969; 4:173–190
    [Google Scholar]
  9. Brenner DJ, Steigerwalt AG, Miklos GV, Fanning GR. Deoxyribonucleic acid relatedness among erwiniae and other Enterobacteriaceae: the soft-rot organisms (genus Pectobacterium Waldee). Int J Syst Bacteriol 1973; 23:205–216 [View Article]
    [Google Scholar]
  10. Hauben L, Moore ERB, Vauterin L, Steenackers M, Mergaert J et al. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst Appl Microbiol 1998; 21:384–397 [View Article] [PubMed]
    [Google Scholar]
  11. Samson R, Legendre JB, Christen R, Fischer-Le Saux M, Achouak W. Transfer of Pectobacterium chrysanthemi (Burkholder et al. 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. Int J Syst Evol Microbiol 2005; 55:1415–1427 [View Article] [PubMed]
    [Google Scholar]
  12. Brady CL, Cleenwerck I, Denman S, Venter SN, Rodrıguez-Palenzuela P et al. Proposal to reclassify Brenneria quercina (Hildebrand & Schroth 1967) Hauben et al. 1999 into a novel genus, Lonsdalea gen. nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. Iberica subsp. nov., and Lonsdalea quercina subsp. britannica subsp. nov., emendation of the description of the genus Brenneria, reclassification of Dickeya dieffenbachiae as Dickeya dadantii subsp. dieffenbachiae comb. nov., and emendation of the description of Dickeya dadantii. Int J Syst Evol Microbiol 2012; 62:1592–1602
    [Google Scholar]
  13. Slawiak M, van Beckhoven J, Speksnijder A, Czajkowski R, Grabe G et al. Biochemical and genetical analysis reveal a new clade of biovar 3 Dickeya spp. strains isolated from potato in Europe. Eur J Plant Pathol 2009; 125:245–261
    [Google Scholar]
  14. van der Wolf JM, Nijhuis EH, Kowalewska MJ, Saddler GS, Parkinson N et al. Dickeya solani sp. nov., a pectinolytic plant-pathogenic bacterium isolated from potato (Solanum tuberosum). Int J Syst Evol Microbiol 2014; 64:768–774 [View Article] [PubMed]
    [Google Scholar]
  15. Tian Y, Zhao Y, Yuan X, Yi J, Fan J et al. Dickeya fangzhongdai sp. nov., a plant-pathogenic bacterium isolated from pear trees (Pyrus pyrifolia. Int J Syst Evol Microbiol 2016; 66:2831–2835 [View Article] [PubMed]
    [Google Scholar]
  16. Alič Š, Van Gijsegem F, Pédron J, Ravnikar M, Dreo T. Diversity within the novel Dickeya fangzhongdai sp., isolated from infected orchids, water and pears. Plant Pathol 2018; 67:1612–1620
    [Google Scholar]
  17. Hugouvieux-Cotte-Pattat N, Brochier-Armanet C, Flandrois JP, Sylvie Reverchon S. Dickeya poaceaphila sp. nov., a plant-pathogenic bacterium isolated from sugar cane (Saccharum officinarum). Int J Syst Evol Microbiol 2020; 70:4508–4514 [View Article]
    [Google Scholar]
  18. Wang X, He SW, Guo HB, Han JG, Thin KK et al. Dickeya oryzae sp. nov., isolated from the roots of rice. Int J Syst Evol Microbiol 2020; 70:4171–4178 [View Article]
    [Google Scholar]
  19. Parkinson N, DeVos P, Pirhonen M, Elphinstone J. Dickeya aquatica sp. nov., isolated from waterways. Int J Syst Evol Microbiol 2014; 64:2264–2266 [View Article] [PubMed]
    [Google Scholar]
  20. Hugouvieux-Cotte-Pattat N, Jacot-des-Combes C, Briolay J. Dickeya lacustris sp. nov., a water-living pectinolytic bacterium isolated from lakes in France. Int J Syst Evol Microbiol 2019; 69:721–726 [View Article] [PubMed]
    [Google Scholar]
  21. Oulghazi S, Pédron J, Cigna J, Lau YY, Moumni M et al. Dickeya undicola sp. nov., a novel species for pectinolytic isolates from surface waters in Europe and Asia. Int J Syst Evol Microbiol 2019; 69:2440–2444 [View Article] [PubMed]
    [Google Scholar]
  22. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24
    [Google Scholar]
  23. Duprey A, Taib N, Leonard S, Garin T, Flandrois JP et al. The phytopathogenic nature of Dickeya aquatica 174/2 and the dynamic early evolution of Dickeya pathogenicity. Environ Microbiol 2019; 21:2809–2835 [View Article] [PubMed]
    [Google Scholar]
  24. Pédron J, Van Gijsegem F. Diversity in the bacterial Dickeya genus grouping plant pathogens and waterways isolates. OBM Genetics 2019; 3:22
    [Google Scholar]
  25. Dickey RS, Victoria JI. Taxonomy and emended description of strains of Erwinia isolated from Musa paradisiaca Lineaus. Int J Syst Bacteriol 1980; 30:129–134
    [Google Scholar]
  26. Pritchard L, Humphris S, Saddler GS, Elphinstone JG, Pirhonen M et al. Draft genome sequences of 17 isolates of the plant pathogenic bacterium Dickeya. Genome Announc 2013; 1:e00978 [View Article]
    [Google Scholar]
  27. Fernandez-Borrero O, Lopez-Duques S. Pudricion acuosa del suedo tallo del platana (Musa paradisiaca) causade por Erwinia paradisiaca n. sp. Cenicafe 1970; 21:3–44
    [Google Scholar]
  28. Marrero G, Schneider KL, Jenkins DM, Alvarez AM. Phylogeny and classification of Dickeya based on multilocus sequence analysis. Int J Syst Evol Microbiol 2013; 63:3524–3539 [View Article]
    [Google Scholar]
  29. Cigna J, Dewaegeneire P, Beury A, Gobert V, Faure D. A gapA PCR sequencing assay for identifying the Dickeya and Pectobacterium potato pathogens. Plant Dis 2017; 101:1278–1282 [View Article] [PubMed]
    [Google Scholar]
  30. Saitou N, Nei M. The neighbour-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
    [Google Scholar]
  31. Barzic MR, Samson R, Trigalet A. Pourriture bactérienne de la tomate cultivée en serre. Ann Phytopathol 1976; 8:237–240
    [Google Scholar]
  32. Bochner BR. Global phenotypic characterization of bacteria. FEMS Microbiol Rev 2009; 33:191–205 [View Article] [PubMed]
    [Google Scholar]
  33. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  34. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  35. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
    [Google Scholar]
  36. 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]
  37. Meier-Kolthoff JPM, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  38. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A genus definition for bacteria and archaea based on a standard genome relatedness index. mBio 2020; 11:e02475 [View Article]
    [Google Scholar]
  39. Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res 2015; 43:6761–6771 [View Article]
    [Google Scholar]
  40. 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]
    [Google Scholar]
  41. Murray CS, Gao Y, Wu M. There is no evidence of a universal genetic boundary among microbial species. bioRxiv 202007.27.223511
    [Google Scholar]
  42. Olm MR, Crits-Christoph A, Diamond S, Lavy A, Matheus Carnevali PB et al. Consistent metagenome-derived metrics verify and delineate bacterial species boundaries. mSystems 2020; 5:e00731-19 [View Article]
    [Google Scholar]
  43. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article]
    [Google Scholar]
  44. Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 2019; 20:238 [View Article] [PubMed]
    [Google Scholar]
  45. Nakamura T, Yamada KD, Tomii K, Katoh K. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 2018; 34:2490–2492 [View Article] [PubMed]
    [Google Scholar]
  46. Notredame C, Higgins DG, Heringa J. T-Coffee: A novel method for multiple sequence alignments. J Mol Biol 2000; 30:205–217
    [Google Scholar]
  47. 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 2019btz305 [View Article]
    [Google Scholar]
  48. Hugouvieux-Cotte-Pattat N, Condemine G, Shevchik VE. Bacterial pectate lyases, structural and functional diversity. Environ Microbiol Rep 2014; 6:427–440 [View Article] [PubMed]
    [Google Scholar]
  49. Reverchon S, Nasser W. Dickeya ecology, environment sensing and regulation of virulence programme. Environ Microbiol Rep 2013; 5:622–636 [View Article] [PubMed]
    [Google Scholar]
  50. Collmer A, Noel T. Keen-pioneer leader in molecular plant pathology. Annu Rev Phytopathol 2007; 45:25–42 [View Article] [PubMed]
    [Google Scholar]
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