1887

Abstract

Several strains of a previously undescribed bacterial species were isolated from mature hybrid trees suffering from bleeding cankers at various geographic locations in the UK. The strains were Gram-negative, facultatively anaerobic, and partial sequencing of the gene revealed that the strains belong to the genus with the closest phylogenetic neighbours being and . Further investigation using a polyphasic approach was undertaken to determine the taxonomic position of the novel species. Phylogenies based on the 16S rRNA gene and multilocus sequence analysis of partial housekeeping gene sequences of , , and revealed that the strains formed an independent cluster within the genus . The phenotypic and chemotaxonomic assays demonstrated that the strains could be differentiated from the closest relatives. Genome analysis of representative strains revealed DNA–DNA hybridization values below the threshold for species delimitation, although the average nucleotide identity values obtained when compared to (95.9–96%) were slightly higher than the suggested cut-off value of 95%. However, as all other data suggests that the strains belong to a novel taxon that can be differentiated from the closest relatives, we propose that the strains represent a novel species in the genus , sp. nov. (type strain WC1b.1=LMG 32575=NCPPB 4697).

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2022-10-07
2024-04-29
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References

  1. Hauben L, Moore ER, Vauterin L, Steenackers M, Mergaert J et al. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst Appl Microbiol 1998; 21:384–397 [View Article]
    [Google Scholar]
  2. Brady CL, Coutinho TA. Brenneria. In Bergey’s Manual of Systematics of Archaea and Bacteria 2021 pp 1–16 [View Article]
    [Google Scholar]
  3. EPPO EPPO Global database; 2022 https://gd.eppo.int accessed 20 January 2022
  4. Denman S, Brady C, Kirk S, Cleenwerck I, Venter S et al. Brenneria goodwinii sp. nov., associated with acute oak decline in the UK. Int J Syst Evol Microbiol 2012; 62:2451–2456 [View Article]
    [Google Scholar]
  5. Surico G, Mugnai L, Pastorelli R, Giovannetti L, Stead DE. Erwinia alni, a new species causing bark cankers of alder (Alnus miller) species. Int J Syst Bacteriol 1996; 46:720–726 [View Article]
    [Google Scholar]
  6. Wilson EE, Zeitoun FM, Fredrickson DL. Bacterial phloem canker, a new disease of persian walnut trees. Phytopathology 1967; 57:618–621
    [Google Scholar]
  7. Denman S, Doonan J, Ransom-Jones E, Broberg M, Plummer S et al. Microbiome and infectivity studies reveal complex polyspecies tree disease in acute oak decline. ISME J 2018; 12:386–399 [View Article] [PubMed]
    [Google Scholar]
  8. Brady C, Hunter G, Kirk S, Arnold D, Denman S. Description of Brenneria roseae sp. nov. and two subspecies, Brenneria roseae subspecies roseae ssp. nov and Brenneria roseae subspecies americana ssp. nov. isolated from symptomatic oak. Syst Appl Microbiol 2014; 37:396–401 [View Article]
    [Google Scholar]
  9. Pigott D. Lime-trees and Basswoods: A biological monograph of the genus Tilia Cambridge: Cambridge University Press; 2012 [View Article]
    [Google Scholar]
  10. De Jaegere T, Hein S, Claessens H. A review of the characteristics of small-leaved lime (Tilia cordata Mill.) and their implications for silviculture in a changing climate. Forests 2012; 7:56 [View Article]
    [Google Scholar]
  11. Rogers K, Sacre K, Goodenough S, Doick K. Valuing london’s urban forest: results of the London i-tree eco project. london 2015
    [Google Scholar]
  12. Hagen-Thorn A, Armolaitis K, Callesen I, Stjernquist I. Macronutrients in tree stems and foliage: a comparative study of six temperate forest species planted at the same sites. Ann For Sci 2004; 61:489–498 [View Article]
    [Google Scholar]
  13. Hagen-Thorn A, Callesen I, Armolaitis K, Nihlgård B. The impact of six European tree species on the chemistry of mineral topsoil in forest plantations on former agricultural land. For Ecol Manage 2004; 195:373–384 [View Article]
    [Google Scholar]
  14. Neirynck J, Mirtcheva S, Sioen G, Lust N. Pseudoplatanus impact of Tilia platyphyllos scop., Fraxinus excelsior on earthworm biomass and physico-chemical properties of a loamy topsoil. For Ecol Manage 2000; 133:275–286 [View Article]
    [Google Scholar]
  15. Pigott C. The growth of lime Tilia cordata in an experimental plantation and its influence on soil development and vegetation. Quaterly J For 1989; 83:14–24
    [Google Scholar]
  16. Kile H. Investigation of the bacterial microbiome of healthy and symptomatic Tilia trees and description of a potential novel Brenneria sp. isolated from symptomatic tissue of Tilia x moltkei canker University of the West of England; 2021
    [Google Scholar]
  17. Niemann S, Pühler A, Tichy HV, Simon R, Selbitschka W. Evaluation of the resolving power of three different DNA fingerprinting methods to discriminate among isolates of a natural Rhizobium meliloti population. J Appl Microbiol 1997; 82:477–484 [View Article]
    [Google Scholar]
  18. Coenye T, Falsen E, Vancanneyt M, Hoste B, Govan JR et al. Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia gilardii sp. nov. Int J Syst Bacteriol 1999; 49 Pt 2:405–413 [View Article] [PubMed]
    [Google Scholar]
  19. Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J et al. Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 2008; 31:447–460 [View Article]
    [Google Scholar]
  20. Okonechnikov K, Golosova O, Fursov M. UGENE team Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 2012; 28:1166–1167 [View Article]
    [Google Scholar]
  21. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
    [Google Scholar]
  22. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article]
    [Google Scholar]
  23. Lefort V, Longueville J-E, Gascuel O. SMS: Smart model selection in PhyML. Mol Biol Evol 2017; 34:2422–2424 [View Article]
    [Google Scholar]
  24. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article]
    [Google Scholar]
  25. Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 1991; 19:6823–6831 [View Article] [PubMed]
    [Google Scholar]
  26. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  27. Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In Lecture Notes in Computer Science (Including Subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics) Springer; 2013 pp 158–170 [View Article]
    [Google Scholar]
  28. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
    [Google Scholar]
  32. 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]
    [Google Scholar]
  33. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
    [Google Scholar]
  34. Farris JS. Estimating phylogenetic trees from distance matrices. The American Naturalist 1972; 106:645–668 [View Article]
    [Google Scholar]
  35. Rosselló-Móra R, Amann R. Past and future species definitions for Bacteria and Archaea. Syst Appl Microbiol 2015; 38:209–216 [View Article] [PubMed]
    [Google Scholar]
  36. Li Y, Zheng M, Wang H, Lin C, Wang X. Brenneria corticis sp. nov., isolated from symptomatic bark of Populus×euramericana canker. Int J Syst Evol Microbiol 2019; 69:63–67 [View Article] [PubMed]
    [Google Scholar]
  37. Palmer M, Steenkamp ET, Blom J, Hedlund BP, Venter SN. All ANIs are not created equal: implications for prokaryotic species boundaries and integration of ANIs into polyphasic taxonomy. Int J Syst Evol Microbiol 2020; 70:2937–2948 [View Article] [PubMed]
    [Google Scholar]
  38. Brady CL, Cleenwerck I, Denman S, Venter SN, Rodríguez-Palenzuela P et al. Proposal to reclassify Brenneria quercina (Hildebrand and Schroth 1967) Hauben et al. 1999 into a new genus, Lonsdalea gen nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. iberica. Int J Syst Evol Microbiol 2012; 62: [View Article]
    [Google Scholar]
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