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Volume 160, Issue 3

Quantitative evaluation of the host-colonizing capabilities of the enteric bacterium using plant and insect hosts Free

Abstract

The genus is a highly diverse group comprising free-living, and both pathogenic and non-pathogenic host-associating species. Pathogenic isolates have been found to infect insects, plants and humans, yet it is unclear whether these isolates have similar pathogenic potential to the free-living environmental populations. Using MLSA of six housekeeping genes, we evaluated the phylogenetic relationships among 115 environmental and clinical (human) isolates representing 11 species. An overlay of the location of isolation onto the resulting tree revealed that clinical and environmental isolates are interspersed, and do not form distinctive groups. We then conducted quantitative growth assays of our isolates using maize, onion and fruit flies as hosts. Notably, most clinical isolates were able to grow in both plant hosts often comparably or even better than the environmental isolates. There were no obvious growth or host colonization patterns that could distinguish those isolates with clinical potential. Growth of an isolate in one host could not be predicted based on its performance in another host, nor could host growth be predicted by phylogeny or source of isolation. This work demonstrates that the host-colonizing capabilities of all species groups is unpredictable, indicating a broader host range and pathogenic potential than currently assumed.

  • Received:
  • Accepted:
  • Published Online:
Funding
This study was supported by the:
  • Natural Sciences and Engineering Council of Canada
  • Canada Foundation for Innovation
  • University of Regina Faculty of Science
© Microbiology Society
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2014-03-01
2024-04-25
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References

  1. Alvarez F. E., Rogge K. J., Tarrand J., Lichtiger B. ( 1995). Bacterial contamination of cellular blood components. A retrospective review at a large cancer center. Ann Clin Lab Sci 25:283–290[PubMed]
     [Google Scholar]
  2. Barash I., Manulis S. ( 2005). Hrp-dependent biotrophic mechanism of virulence: how has it evolved in tumorigenic bacteria. Phytoparasitica 33:317–324 [View Article]
     [Google Scholar]
  3. Basset A., Khush R. S., Braun A., Gardan L., Boccard F., Hoffmann J. A., Lemaitre B. ( 2000). The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci U S A 97:3376–3381 [View Article][PubMed]
     [Google Scholar]
  4. Basset A., Tzou P., Lemaitre B., Boccard F. ( 2003). A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster . EMBO Rep 4:205–209 [View Article][PubMed]
     [Google Scholar]
  5. Bennett S. N., McNeil M. M., Bland L. A., Arduino M. J., Villarino M. E., Perrotta D. M., Burwen D. R., Welbel S. F., Pegues D. A. & other authors ( 1995). Postoperative infections traced to contamination of an intravenous anesthetic, propofol. N Engl J Med 333:147–154 [View Article][PubMed]
     [Google Scholar]
  6. Bicudo E. L., Macedo V. O., Carrara M. A., Castro F. F. S., Rage R. I. ( 2007). Nosocomial outbreak of Pantoea agglomerans in a pediatric urgent care center. Braz J Infect Dis 11:281–284 [View Article][PubMed]
     [Google Scholar]
  7. Brady C., Cleenwerck I., Venter S., Vancanneyt M., Swings J., Coutinho T. ( 2008). Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 31:447–460 [View Article][PubMed]
     [Google Scholar]
  8. Brandl M. T., Lindow S. E. ( 1998). Contribution of indole-3-acetic acid production to the epiphytic fitness of Erwinia herbicola . Appl Environ Microbiol 64:3256–3263[PubMed]
     [Google Scholar]
  9. Brandl M. T., Quiñones B., Lindow S. E. ( 2001). Heterogeneous transcription of an indoleacetic acid biosynthetic gene in Erwinia herbicola on plant surfaces. Proc Natl Acad Sci U S A 98:3454–3459 [View Article][PubMed]
     [Google Scholar]
  10. Braun-Kiewnick A., Jacobsen B. J., Sands D. C. ( 2000). Biological control of Pseudomonas syringae pv. syringae, the causal agent of basal kernel blight of barley, by antagonistic Pantoea agglomerans . Phytopathology 90:368–375 [View Article][PubMed]
     [Google Scholar]
  11. Brown B. J., Leff L. G. ( 1996). Comparison of fatty acid methyl ester analysis with the use of API 20E and NFT strips for identification of aquatic bacteria. Appl Environ Microbiol 62:2183–2185[PubMed]
     [Google Scholar]
  12. Castonguay-Vanier J., Vial L., Tremblay J., Déziel E. ( 2010). Drosophila melanogaster as a model host for the Burkholderia cepacia complex. PLoS ONE 5:e11467 [View Article][PubMed]
     [Google Scholar]
  13. Choi O., Lim J. Y., Seo Y.-S., Hwang I., Kim J. ( 2012). Complete genome sequence of the rice pathogen Pantoea ananatis strain PA13. J Bacteriol 194:531 [View Article][PubMed]
     [Google Scholar]
  14. Coplin D. L., Frederick R. D., Majerczak D. R., Haas E. S. ( 1986). Molecular cloning of virulence genes from Erwinia stewartii . J Bacteriol 168:619–623[PubMed]
     [Google Scholar]
  15. Coplin D. L., Majerczak D. R., Zhang Y. X., Kim W. S., Jock S., Geider K. ( 2002). Identification of Pantoea stewartii subsp stewartii by PCR and strain differentiation by PFGE. Plant Dis 86:304–311 [View Article]
     [Google Scholar]
  16. Cosimo M. a. J.-M., R. ( 2005). Evolution and integration of innate immune systems from fruit flies to man: lessons and questions. J Endotoxin Res 11:243–248 [View Article]
     [Google Scholar]
  17. Coutinho T. A., Venter S. N. ( 2009). Pantoea ananatis: an unconventional plant pathogen. Mol Plant Pathol 10:325–335 [View Article][PubMed]
     [Google Scholar]
  18. Cruz A. T., Cazacu A. C., Allen C. H. ( 2007). Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol 45:1989–1992 [View Article][PubMed]
     [Google Scholar]
  19. D’Argenio D. A., Gallagher L. A., Berg C. A., Manoil C. ( 2001). Drosophila as a model host for Pseudomonas aeruginosa infection. J Bacteriol 183:1466–1471 [View Article][PubMed]
     [Google Scholar]
  20. De Champs C., Le Seaux S., Dubost J. J., Boisgard S., Sauvezie B., Sirot J. ( 2000). Isolation of Pantoea agglomerans in two cases of septic monoarthritis after plant thorn and wood sliver injuries. J Clin Microbiol 38:460–461[PubMed]
     [Google Scholar]
  21. De Maayer P., Chan W. Y., Venter S. N., Toth I. K., Birch P. R. J., Joubert F., Coutinho T. A. ( 2010). Genome sequence of Pantoea ananatis LMG20103, the causative agent of Eucalyptus blight and dieback. J Bacteriol 192:2936–2937 [View Article][PubMed]
     [Google Scholar]
  22. De Maayer P., Chan W. Y., Rezzonico F., Bühlmann A., Venter S. N., Blom J., Goesmann A., Frey J. E., Smits T. H. & other authors ( 2012). Complete genome sequence of clinical isolate Pantoea ananatis LMG 5342. J Bacteriol 194:1615–1616 [View Article][PubMed]
     [Google Scholar]
  23. Delétoile A., Decré D., Courant S., Passet V., Audo J., Grimont P., Arlet G., Brisse S. ( 2009). Phylogeny and identification of Pantoea species and typing of Pantoea agglomerans strains by multilocus gene sequencing. J Clin Microbiol 47:300–310 [View Article][PubMed]
     [Google Scholar]
  24. Dionne M. S., Schneider D. S. ( 2008). Models of infectious diseases in the fruit fly Drosophila melanogaster . Dis Model Mech 1:43–49 [View Article][PubMed]
     [Google Scholar]
  25. Edens D. G., Gitaitis R. D., Sanders F. H., Nischwitz C. ( 2006). First report of Pantoea agglomerans causing a leaf blight and bulb rot of onions in Georgia. Plant Dis 90:1551 [View Article]
     [Google Scholar]
  26. Edgar R. C. ( 2004). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  27. Flatauer F. E., Khan M. A. ( 1978). Septic arthritis caused by Enterobacter agglomerans . Arch Intern Med 138:788 [View Article][PubMed]
     [Google Scholar]
  28. Francis C. A., Obraztsova A. Y., Tebo B. M. ( 2000). Dissimilatory metal reduction by the facultative anaerobe Pantoea agglomerans SP1. Appl Environ Microbiol 66:543–548 [View Article][PubMed]
     [Google Scholar]
  29. Gitaitis R. D., Walcott R. R., Wells M. L., Perez J. C. D., Sanders F. H. ( 2003). Transmission of Pantoea ananatis, causal agent of center rot of onion, by tobacco thrips, Frankliniella fusca . Plant Dis 87:675–678 [View Article]
     [Google Scholar]
  30. Gitaitis R. D., Sanders F. H., Walcott R. R., Burrell D. ( 2004). Bacterial leaf blight and bulb rot of onion in Peru caused by Pantoea agglomerans and P. ananatis . Phytopathology 94:S145
     [Google Scholar]
  31. Goszczynska T., Moloto V. M., Venter S. N., Coutinho T. A. ( 2006). Isolation and identification of Pantoea ananatis from onion seed in South Africa. Seed Sci Technol 34:655–668 [CrossRef]
     [Google Scholar]
  32. Goszczynska T., Moloto V. M., Coutinho T. A. ( 2007). Bacterial blights of leek and onion caused by Pseudomonas syringae . S Afr J Sci 103:vii
     [Google Scholar]
  33. Habsah H., Zeehaida M., Van Rostenberghe H., Noraida R., Wan Pauzi W. I., Fatimah I., Rosliza A. R., Nik Sharimah N. Y., Maimunah H. ( 2005). An outbreak of Pantoea spp. in a neonatal intensive care unit secondary to contaminated parenteral nutrition. J Hosp Infect 61:213–218 [View Article][PubMed]
     [Google Scholar]
  34. Hara Y., Kadotani N., Izui H., Katashkina J. I., Kuvaeva T. M., Andreeva I. G., Golubeva L. I., Malko D. B., Makeev V. J. & other authors ( 2012). The complete genome sequence of Pantoea ananatis AJ13355, an organism with great biotechnological potential. Appl Microbiol Biotechnol 93:331–341 [View Article][PubMed]
     [Google Scholar]
  35. Hoffmann J. A. ( 2003). The immune response of Drosophila . Nature 426:33–38 [View Article][PubMed]
     [Google Scholar]
  36. Hong K.-W., Gan H. M., Low S.-M., Lee P. K. Y., Chong Y.-M., Yin W.-F., Chan K.-G. ( 2012). Draft genome sequence of Pantoea sp. strain A4, a Rafflesia-associated bacterium that produces N-acylhomoserine lactones as quorum-sensing molecules. J Bacteriol 194:6610 [View Article][PubMed]
     [Google Scholar]
  37. Kim H. J., Lee J. H., Kang B. R., Rong X., McSpadden Gardener B. B., Ji H. J., Park C.-S., Kim Y. C. ( 2012). Draft genome sequence of Pantoea ananatis B1-9, a nonpathogenic plant growth-promoting bacterium. J Bacteriol 194:729 [View Article][PubMed]
     [Google Scholar]
  38. Kirzinger M. W. B., Stavrinides J. ( 2012). Host specificity determinants as a genetic continuum. Trends Microbiol 20:88–93 [View Article][PubMed]
     [Google Scholar]
  39. Kirzinger M. W. B., Nadarasah G., Stavrinides J. ( 2011). Insights into cross-kingdom plant pathogenic bacteria. Genes 2:980–997 [View Article]
     [Google Scholar]
  40. Kratz A., Greenberg D., Barki Y., Cohen E., Lifshitz M. ( 2003). Pantoea agglomerans as a cause of septic arthritis after palm tree thorn injury; case report and literature review. Arch Dis Child 88:542–544 [View Article][PubMed]
     [Google Scholar]
  41. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. & other authors ( 2007). clustal w and clustal_x version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
     [Google Scholar]
  42. Lauzon C. R., McCombs S. D., Potter S. E., Peabody N. C. ( 2009). Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the Mediterranean fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:85–95 [View Article]
     [Google Scholar]
  43. Lemaitre B., Reichhart J. M., Hoffmann J. A. ( 1997). Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci U S A 94:14614–14619 [View Article][PubMed]
     [Google Scholar]
  44. Lindow S. E., Arny D. C., Upper C. D. ( 1978). Erwinia herbicola – bacterial ice nucleus active in increasing frost injury to corn. Phytopathology 68:523–527 [View Article]
     [Google Scholar]
  45. Loncaric I., Heigl H., Licek E., Moosbeckhofer R., Busse H. J., Rosengarten R. ( 2009). Typing of Pantoea agglomerans isolated from colonies of honey bees (Apis mellifera) and culturability of selected strains from honey. Apidologie 40:40–54 [View Article]
     [Google Scholar]
  46. Marcell L. M., Beattie G. A. ( 2002). Effect of leaf surface waxes on leaf colonization by Pantoea agglomerans and Clavibacter michiganensis . Mol Plant Microbe Interact 15:1236–1244 [View Article][PubMed]
     [Google Scholar]
  47. Martinelli C., Reichhart J. M. ( 2005). Evolution and integration of innate immune systems from fruit flies to man: lessons and questions. J Endotoxin Res 11:243–248[PubMed] [CrossRef]
     [Google Scholar]
  48. Matsaniotis N. S., Syriopoulou V. P., Theodoridou M. C., Tzanetou K. G., Mostrou G. I. ( 1984). Enterobacter sepsis in infants and children due to contaminated intravenous fluids. Infect Control 5:471–477[PubMed]
     [Google Scholar]
  49. Matsuzawa T., Mori K., Kadowaki T., Shimada M., Tashiro K., Kuhara S., Inagawa H., Soma G., Takegawa K. ( 2012). Genome sequence of Pantoea agglomerans strain IG1. J Bacteriol 194:1258–1259 [View Article][PubMed]
     [Google Scholar]
  50. Medrano E. G., Bell A. A. ( 2012). Genome sequence of Pantoea sp. strain Sc 1, an opportunistic cotton pathogen. J Bacteriol 194:3019 [View Article][PubMed]
     [Google Scholar]
  51. Morohoshi T., Nakamura Y., Yamazaki G., Ishida A., Kato N., Ikeda T. ( 2007). The plant pathogen Pantoea ananatis produces N-acylhomoserine lactone and causes center rot disease of onion by quorum sensing. J Bacteriol 189:8333–8338 [View Article][PubMed]
     [Google Scholar]
  52. Nadarasah G., Stavrinides J. ( 2011). Insects as alternative hosts for phytopathogenic bacteria. FEMS Microbiol Rev 35:555–575 [View Article][PubMed]
     [Google Scholar]
  53. Nuclo R. L., Johnson K. B., Stockwell V. O., Sugar D. ( 1998). Secondary colonization of pear blossoms by two bacterial antagonists of the fire blight pathogen. Plant Dis 82:661–668 [View Article]
     [Google Scholar]
  54. Rezzonico F., Smits T. H., Montesinos E., Frey J. E., Duffy B. ( 2009). Genotypic comparison of Pantoea agglomerans plant and clinical strains. BMC Microbiol 9:204 [View Article][PubMed]
     [Google Scholar]
  55. Robacker D. C., Lauzon C. R. ( 2002). Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly. J Chem Ecol 28:1549–1563 [View Article][PubMed]
     [Google Scholar]
  56. Robacker D. C., Lauzon C. R., He X. ( 2004). Volatiles production and attractiveness to the Mexican fruit fly of Enterobacter agglomerans isolated from apple maggot and Mexican fruit flies. J Chem Ecol 30:1329–1347 [View Article][PubMed]
     [Google Scholar]
  57. Roper M. C. ( 2011). Pantoea stewartii subsp. stewartii: lessons learned from a xylem-dwelling pathogen of sweet corn. Mol Plant Pathol 12:628–637 [View Article][PubMed]
     [Google Scholar]
  58. Sabaratnam S., Beattie G. A. ( 2003). Differences between Pseudomonas syringae pv. syringae B728a and Pantoea agglomerans BRT98 in epiphytic and endophytic colonization of leaves. Appl Environ Microbiol 69:1220–1228 [View Article][PubMed]
     [Google Scholar]
  59. Smits T. H. M., Rezzonico F., Kamber T., Goesmann A., Ishimaru C. A., Stockwell V. O., Frey J. E., Duffy B. ( 2010). Genome sequence of the biocontrol agent Pantoea vagans strain C9-1. J Bacteriol 192:6486–6487 [View Article][PubMed]
     [Google Scholar]
  60. Stavrinides J. ( 2009). Origin and evolution of phytopathogenic bacteria. Plant Pathogenic Bacteria: Genomics and Molecular Biology330 Jackson R. W. Poole: Caister Academic Press;
     [Google Scholar]
  61. Stavrinides J., No A., Ochman H. ( 2010). A single genetic locus in the phytopathogen Pantoea stewartii enables gut colonization and pathogenicity in an insect host. Environ Microbiol 12:147–155 [View Article][PubMed]
     [Google Scholar]
  62. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. ( 2011). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  63. Ulloa-Gutierrez R., Moya T., Avila-Aguero M. L. ( 2004). Pantoea agglomerans and thorn-associated suppurative arthritis. Pediatr Infect Dis J 23:690 [View Article][PubMed]
     [Google Scholar]
  64. Vincent K., Szabo R. M. ( 1988). Enterobacter agglomerans osteomyelitis of the hand from a rose thorn. A case report. Orthopedics 11:465–467[PubMed]
     [Google Scholar]
  65. Völksch B., Thon S., Jacobsen I. D., Gube M. ( 2009). Polyphasic study of plant- and clinic-associated Pantoea agglomerans strains reveals indistinguishable virulence potential. Infect Genet Evol 9:1381–1391 [View Article][PubMed]
     [Google Scholar]
  66. von Bodman S. B., Majerczak D. R., Coplin D. L. ( 1998). A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii . Proc Natl Acad Sci U S A 95:7687–7692 [View Article][PubMed]
     [Google Scholar]
  67. Wodzinski R. S., Paulin J. P. ( 1994). Frequency and diversity of antibiotic production by putative Erwinia herbicola strains. J Appl Bacteriol 76:603–607 [View Article]
     [Google Scholar]
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Quantitative evaluation of the host-colonizing capabilities of the enteric bacterium Pantoea using plant and insect hosts
Microbiology 160, 602 (2014); https://doi.org/10.1099/mic.0.073452-0
/content/journal/micro/10.1099/mic.0.073452-0
/content/journal/micro/10.1099/mic.0.073452-0
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