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Volume 70, Issue 4

sp. nov., having a SPI-1-like Type III secretion system and low virulence Open Access

Abstract

strains isolated from potato stems in Finland, Poland and the Netherlands were subjected to polyphasic analyses to characterize their genomic and phenotypic features. Phylogenetic analysis based on 382 core proteins showed that the isolates clustered closest to but could be divided into two clades. Average nucleotide identity (ANI) analysis revealed that the isolates in one of the clades included the type strain, whereas the second clade was at the border of the species with a 96 % ANI value. genome-to-genome comparisons between the isolates revealed values below 70%, patristic distances based on 1294 core proteins were at the level observed between closely related species, and the two groups of bacteria differed in genome size, G+C content and results of amplified fragment length polymorphism and Biolog analyses. Comparisons between the genomes revealed that the isolates of the atypical group contained SPI-1-type Type III secretion island and genes coding for proteins known for toxic effects on nematodes or insects, and lacked many genes coding for previously characterized virulence determinants affecting rotting of plant tissue by soft rot bacteria. Furthermore, the atypical isolates could be differentiated from by their low virulence, production of antibacterial metabolites and a citrate-negative phenotype. Based on the results of a polyphasic approach including genome-to-genome comparisons, biochemical and virulence assays, presented in this report, we propose delineation of the atypical isolates as a novel species , for which the isolate s0421 (CFBP 8630=LMG 30828) is suggested as a type strain.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): Pectobacterium , Pectobacterium parvum , potato , Salmonella SPI-1 T3SS , soft rot and virulence
Funding
This study was supported by the:
  • Ministerstwo Nauki i Szkolnictwa Wyższego (PL) (Award MNiSW-DS-6002-4693-23/WA/12)
    • Principle Award Recipient: Krzysztof Waleron
  • Narodowym Centrum Nauki (PL) (Award 2015/17/B/NZ9/01730)
    • Principle Award Recipient: Malgorzata Waleron
  • Maa- ja MetsätalousministeriÖ (Award 1966/03.01.01./2015)
    • Principle Award Recipient: Minna Ursula Pirhonen
  • Uudenmaan Rahasto
    • Principle Award Recipient: Miia Pasanen
  • Emil Aaltosen Säätiö
    • Principle Award Recipient: Miia Pasanen
  • Federal Public Planning Service - Science Policy, Belgium
    • Principle Award Recipient: Peter Vandamme
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.

Erratum

An erratum has been published for this content:
Corrigendum: sp. nov., having a SPI-1-like Type III secretion system and low virulence
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References

  1. 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]
     [Google Scholar]
  2. Ma B, Hibbing ME, Kim H-S, Reedy RM, Yedidia I et al. Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya . Phytopathology 2007; 97:1150–1163 [View Article]
     [Google Scholar]
  3. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Analytical Methods 2016; 8:12–24 [View Article]
     [Google Scholar]
  4. Portier P, Pédron J, Taghouti G, Fischer-Le Saux M, Caullireau E et al. Elevation of Pectobacterium carotovorum subsp. odoriferum to species level as Pectobacterium odoriferum sp. nov., proposal of Pectobacterium brasiliense sp. nov. and Pectobacterium actinidiae sp. nov., emended description of Pectobacterium carotovorum and description of Pectobacterium versatile sp. nov., isolated from streams and symptoms on diverse plants . Int J Syst Evol Microbiol 2019; 69:3207–3216 [View Article]
     [Google Scholar]
  5. Waleron M, Misztak A, Waleron M, Jonca J, Furmaniak M et al. Pectobacterium polonicum sp. nov. isolated from vegetable fields. Int J Syst Evol Microbiol 2019; 69:1751–1759 [View Article]
     [Google Scholar]
  6. Sarfraz S, Riaz K, Oulghazi S, Cigna J, Sahi ST et al. Pectobacterium punjabense sp. nov., isolated from blackleg symptoms of potato plants in Pakistan. Int J Syst Evol Microbiol 2018; 68:3551–3556 [View Article]
     [Google Scholar]
  7. Pédron J, Bertrand C, Taghouti G, Portier P, Barny MA. Pectobacterium aquaticum sp. nov., isolated from waterways. Int J Syst Evol Microbiol 2019; 69:745–751 [View Article]
     [Google Scholar]
  8. Dees MW, Lysøe E, Rossmann S, Perminow J, Brurberg MB. Pectobacterium polaris sp. nov., isolated from potato (Solanum tuberosum). Int J Syst Evol Microbiol 2017; 67:5222–5229 [View Article]
     [Google Scholar]
  9. Waleron M, Misztak A, Waleron M, Franczuk M, Wielgomas B et al. Transfer of Pectobacterium carotovorum subsp. carotovorum strains isolated from potatoes grown at high altitudes to Pectobacterium peruviense sp. nov. Syst Appl Microbiol 2018; 41:85–93 [View Article]
     [Google Scholar]
  10. Pitman AR, Harrow SA, Visnovsky SB. Genetic characterisation of Pectobacterium wasabiae causing soft rot disease of potato in New Zealand. Eur J Plant Pathol 2010; 126:423–435 [View Article]
     [Google Scholar]
  11. Nykyri J, Niemi O, Koskinen P, Nokso-Koivisto J, Pasanen M et al. Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog 2012; 8:e1003013 [View Article]
     [Google Scholar]
  12. Khayi S, Cigna J, Chong TM, Quêtu-Laurent A, Chan KG et al. Transfer of the potato plant isolates of Pectobacterium wasabiae to Pectobacterium parmentieri sp. nov. Int J Syst Evol Microbiol 2016; 66:5379–5383 [View Article]
     [Google Scholar]
  13. Niemi O, Laine P, Koskinen P, Pasanen M, Pennanen V et al. Genome sequence of the model plant pathogen Pectobacterium carotovorum SCC1. Stand Genomic Sci 2017; 12:87 [View Article]
     [Google Scholar]
  14. Shirshikov FV, Korzhenkov AA, Miroshnikov KK, Kabanova AP, Barannik AP et al. Draft genome sequences of new genomospecies "Candidatus Pectobacterium maceratum" strains, which cause soft rot in plants. Genome Announc 2018; 6:e00260-18–18 [View Article]
     [Google Scholar]
  15. Pasanen M, Laurila J, Brader G, Palva ET, Ahola V et al. Characterisation of Pectobacterium wasabiae and Pectobacterium carotovorum subsp. carotovorum isolates from diseased potato plants in Finland. Ann Appl Biol 2013; 163:403–419 [View Article]
     [Google Scholar]
  16. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013; 4:2304 [View Article]
     [Google Scholar]
  17. 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]
     [Google Scholar]
  18. Meier-Kolthoff JP, 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]
     [Google Scholar]
  19. Auch AF, von Jan M, Klenk HP, 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]
     [Google Scholar]
  20. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article]
     [Google Scholar]
  21. Fourment M, Gibbs MJ. PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol Biol 2006; 6:1 [View Article]
     [Google Scholar]
  22. Chimetto LA, Cleenwerck I, Brocchi M, Willems A, De Vos P et al. Marinomonas brasilensis sp. nov., isolated from the coral Mussismilia hispida, and reclassification of Marinomonas basaltis as a later heterotypic synonym of Marinomonas communis . Int J Syst Evol Microbiol 2011; 61:1170–1175 [View Article]
     [Google Scholar]
  23. Sistek V, Maheux AF, Boissinot M, Bernard KA, Cantin P et al. Enterococcus ureasiticus sp. nov. and Enterococcus quebecensis sp. nov., isolated from water. Int J Syst Evol Microbiol 2012; 62:1314–1320 [View Article]
     [Google Scholar]
  24. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. Blast ring image generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article]
     [Google Scholar]
  25. Galata V, Fehlmann T, Backes C, Keller A. PLSDB: a resource of complete bacterial plasmids. Nucleic Acids Res 2019; 47:D195–D202 [View Article]
     [Google Scholar]
  26. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003; 13:2178–2189 [View Article]
     [Google Scholar]
  27. Lara-Ramírez EE, Segura-Cabrera A, Guo X, Yu G, García-Pérez CA et al. New implications on genomic adaptation derived from the Helicobacter pylori genome comparison. PLoS One 2011; 6:e17300 [View Article]
     [Google Scholar]
  28. Dundore-Arias JP, Groves RL, Barak JD. Influence of prgH on the Persistence of Ingested Salmonella enterica in the Leafhopper Macrosteles quadrilineatus . Appl Environ Microbiol 2015; 81:6345–6354 [View Article]
     [Google Scholar]
  29. Correa VR, Majerczak DR, Ammar E-D, Merighi M, Pratt RC et al. The bacterium Pantoea stewartii uses two different type III secretion systems to colonize its plant host and insect vector. Appl Environ Microbiol 2012; 78:6327–6336 [View Article]
     [Google Scholar]
  30. Egan F, Barret M, O'Gara F. The SPI-1-like type III secretion system: more roles than you think. Front Plant Sci 2014; 5:34 [View Article]
     [Google Scholar]
  31. Hurst MRH, Beattie A, Jones SA, Laugraud A, van Koten C et al. Serratia proteamaculans Strain AGR96X Encodes an Antifeeding Prophage (Tailocin) with Activity against Grass Grub (Costelytra giveni) and Manuka Beetle (Pyronota Species) Larvae. Appl Environ Microbiol 2018; 84:10 [View Article]
     [Google Scholar]
  32. Huber B, Feldmann F, Köthe M, Vandamme P, Wopperer J et al. Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans . Infect Immun 2004; 72:7220–7230 [View Article]
     [Google Scholar]
  33. Styer KL, Hopkins GW, Bartra SS, Plano GV, Frothingham R et al. Yersinia pestis kills Caenorhabditis elegans by a biofilm-independent process that involves novel virulence factors. EMBO Rep 2005; 6:992–997 [View Article]
     [Google Scholar]
  34. Rossmann S, Dees MW, Perminow J, Meadow R, Brurberg MB. Soft rot Enterobacteriaceae are carried by a large range of insect species in potato fields. Appl Environ Microbiol 2018; 84:pii:e00281–18 [View Article]
     [Google Scholar]
  35. Joynson R, Swamy A, Bou PA, Chapuis A, Ferry N. Characterization of cellulolytic activity in the gut of the terrestrial land slug Arion ater: Biochemical identification of targets for intensive study. Comp Biochem Physiol B Biochem Mol Biol 2014; 177-178:29–35 [View Article]
     [Google Scholar]
  36. Nykyri J, Fang X, Dorati F, Bakr R, Pasanen M et al. Evidence that nematodes may vector the soft rot-causing enterobacterial phytopathogens. Plant Pathology 2014; 63:747–757 [View Article]
     [Google Scholar]
  37. Mongae A, Kubheka GC, Moleleki N, Moleleki LN. The use of fluorescent reporter protein tagging to study the interaction between Root-Knot Nematodes and Soft Rot Enterobacteriaceae . Lett Appl Microbiol 2013; 56:258–263 [View Article]
     [Google Scholar]
  38. Giddens SR, Feng Y, Mahanty HK. Characterization of a novel phenazine antibiotic gene cluster in Erwinia herbicola Eh1087. Mol Microbiol 2002; 45:769–783 [View Article]
     [Google Scholar]
  39. Pierson LS, Pierson EA. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol 2010; 86:1659–1670 [View Article]
     [Google Scholar]
  40. Hogan CS, Mole BM, Grant SR, Willis DK, Charkowski AO. The type III secreted effector DspE is required early in solanum tuberosum leaf infection by Pectobacterium carotovorum to cause cell death, and requires Wx(3-6)D/E motifs. PLoS One 2013; 8:e65534 [View Article]
     [Google Scholar]
  41. Mattinen L, Somervuo P, Nykyri J, Nissinen R, Kouvonen P et al. Microarray profiling of host-extract-induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum . Microbiology 2008; 154:2387–2396 [View Article]
     [Google Scholar]
  42. Urbany C, Neuhaus HE. Citrate uptake into Pectobacterium atrosepticum is critical for bacterial virulence. Mol Plant Microbe Interact 2008; 21:547–554 [View Article]
     [Google Scholar]
  43. Turkovicova L, Smidak R, Jung G, Turna J, Lubec G et al. Proteomic analysis of the TERC interactome: novel links to tellurite resistance and pathogenicity. J Proteomics 2016; 136:167–173 [View Article]
     [Google Scholar]
  44. Espinel IC, Guerra PR, Jelsbak L. Multiple roles of putrescine and spermidine in stress resistance and virulence of Salmonella enterica serovar Typhimurium. Microb Pathog 2016; 95:117–123 [View Article]
     [Google Scholar]
  45. Freeman ZN, Dorus S, Waterfield NR. The KdpD/KdpE two-component system: integrating K⁺ homeostasis and virulence. PLoS Pathog 2013; 9:e1003201 [View Article]
     [Google Scholar]
  46. Chatterjee A, McEvoy JL, Chambost JP, Blasco F, Chatterjee AK. Nucleotide sequence and molecular characterization of pnlA, the structural gene for damage-inducible pectin lyase of Erwinia carotovora subsp. carotovora 71. J Bacteriol 1991; 173:1765–1769 [View Article]
     [Google Scholar]
  47. Pirhonen M, Saarilahti H, Karlsson MB, Palva ET. Identification of Pathogenicity Determinants of Erwinia carotovora subsp. carotovora by Transposon Mutagenesis. MPMI 1991; 4:276–283 [View Article]
     [Google Scholar]
  48. Valente RS, Xavier KB. The Trk Potassium Transporter Is Required for RsmB-Mediated Activation of Virulence in the Phytopathogen Pectobacterium wasabiae . J Bacteriol 2016; 198:248–255 [View Article]
     [Google Scholar]
  49. Shi Z, Wang Q, Li Y, Liang Z, Xu L et al. Putrescine Is an Intraspecies and Interkingdom Cell-Cell Communication Signal Modulating the Virulence of Dickeya zeae . Front Microbiol 2019; 10:10 [View Article]
     [Google Scholar]
  50. De Boer SH, Kelman A. Erwinia soft rot group. In Schaad NW, Jones JB. (editors) Laboratory Guide for Identification of Plant Pathogenic Bacteria, 3rd edn. St. Paul, MN, USA: American Phytopathological Society; 2002 pp 56–57
     [Google Scholar]
  51. Hyman LJ, Toth IK, Pérombelon MCM. Isolation and identification. In Pérombelon MCM, Van der Wolf JM. (editors) Methods for the Detection and Quantification of Erwinia carotovora subsp. atroseptica (Pectobacterium carotovorum subsp. atrosepticum) on Potatoes: A Laboratory Manual Dundee, Scotland, UK: Scottish Crop Research Institute Occasional Publication No. 10; 2002 pp 66–71
     [Google Scholar]
  52. De Boer SH, Copeman RJ, Vruggink H. Serogroups of Erwinia carotovora potato strains determined with diffusible somatic antigens. Phytopathology 1979; 69:316–319 [View Article]
     [Google Scholar]
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Pectobacterium parvum sp. nov., having a Salmonella SPI-1-like Type III secretion system and low virulence
Int J Syst Evol Microbiol 70, 2440 (2020); https://doi.org/10.1099/ijsem.0.004057
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