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Enterobacter cloacae, an Emerging Plant-Pathogenic Bacterium Affecting Chili Pepper Seedlings

  • Garcia-Gonzalez, Tanahiri (Universidad Autonoma de Chihuahua, Chihuahua, Campus 1) ;
  • Saenz-Hidalgo, Hilda Karina (Universidad Autonoma de Chihuahua, Chihuahua, Campus 1) ;
  • Silva-Rojas, Hilda Victoria (Colegio de Postgraduados, Campus Montecillo) ;
  • Morales-Nieto, Carlos (Universidad Autonoma de Chihuahua, Facultad de Zootecnia y Ecologia) ;
  • Vancheva, Taca (UMR Interactions Plantes Microorganismes Environnement (IPME), IRD-Cirad-Universite Montpellier) ;
  • Koebnik, Ralf (UMR Interactions Plantes Microorganismes Environnement (IPME), IRD-Cirad-Universite Montpellier) ;
  • Avila-Quezada, Graciela Dolores (Universidad Autonoma de Chihuahua, Facultad de Zootecnia y Ecologia)
  • Received : 2017.06.25
  • Accepted : 2017.10.13
  • Published : 2018.02.01

Abstract

A previously unreported bacterial disease on chili pepper (Capsicum annuum L.) seedlings affecting as many as 4% of seedlings was observed in greenhouses in Chihuahua, Mexico (Delicias and Meoqui counties). Initial lesions appeared as irregular small spots on leaves and brown necrosis at margins tips were observed. Later, the spots became necrotic with a chlorotic halo. Advanced disease was associated with defoliation. A Gram negative, rod-shaped bacterium was isolated from diseased chili pepper seedlings. Three inoculation methods revealed that isolated strains produce foliage symptoms, similar to those observed in naturally infected seedlings. Pathogenic strains that caused symptoms in inoculated seedlings were re-isolated and identified to fulfill koch's postulate. Polyphasic approaches for identification including biochemical assays (API 20E and 50CH), carbon source utilization profiling (Biolog) and 16S rDNA, hsp60 and rpoB sequence analysis were done. Enterobacter cloacae was identified as the causal agent of this outbreak on chili pepper seedlings.

Keywords

bacterium;Capsicum annuum L.;hsp60;rpoB;16S rDNA

References

  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
  2. Bergey, D. H. and Holt, J. G. 1994. Bergey's manual of determinative bacteriology. Wilkins and Wilkins, Baltimore, USA.
  3. Bishop, A. L. and Davis, R. M. 1990. Internal decay of onions caused by Enterobacter cloacae. Plant Dis. 74:692-694. https://doi.org/10.1094/PD-74-0692
  4. Carter, J. C. 1945. Wetwood of elms. Ill. Nat. Hist. Surv. Bull. 23:407-448.
  5. Case, R. J., Boucher, Y., Dahllof, I., Holmstrom, C., Doolittle, W. F. and Kjelleberg, S. 2007. Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl. Environ. Microbiol. 73:278-288. https://doi.org/10.1128/AEM.01177-06
  6. Cother, E. J. and Dowling, V. 1986. Bacteria associated with internal breakdown of onion bulbs and their possible role in disease expression. Plant Pathol. 35:329-336. https://doi.org/10.1111/j.1365-3059.1986.tb02023.x
  7. Dalben, M., Varkulja, G., Basso, M., Krebs, V. L., Gibelli, M. A., van der Heijden, I., Rossi, F., Duboc, G., Levin, A. S. and Costa, S. F. 2008. Investigation of an outbreak of Enterobacter cloacae in a neonatal unit and review of the literature. J. Hosp. Infect. 70:7-14. https://doi.org/10.1016/j.jhin.2008.05.003
  8. Davin-Regli, A. and Pages, J. M. 2015. Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Front. Microbiol. 6:392.
  9. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M. and Gascuel, O. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:465-469. https://doi.org/10.1093/nar/gkn180
  10. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. https://doi.org/10.1093/nar/gkh340
  11. Fanaro, S., Chierici, R., Guerrini, P. and Vigi, V. 2003. Intestinal microflora in early infancy: composition and development. Acta Paediatr. 91:48-55.
  12. George, M., Potty, V. P. and Jayasankar, N. P. 1976. Association of Enterobacter with coconut root (wilt) disease. Curr. Sci. 45:677-678.
  13. Hormaeche, E. and Edwards, P. R. 1960. A proposed genus Enterobacter. Int. Bull. Bacteriol. Nomencl. Taxon. 10:71-74.
  14. Hoffmann, H. and Roggenkamp, A. 2003. Population genetics of the nomenspecies Enterobacter cloacae. Appl. Environ. Microbiol. 69:5306-5318. https://doi.org/10.1128/AEM.69.9.5306-5318.2003
  15. Li, D., Li, Z., Yu, J., Cao, N., Liu, R. and Yang, M. 2010. Characterization of bacterial community structure in a drinking water distribution system during an occurrence of red water. Appl. Environ. Microbiol. 76:7171-7180. https://doi.org/10.1128/AEM.00832-10
  16. Liu, W. Y., Wong, C. F., Chung, K. M., Jiang, J. W. and Leung, F. C. 2013. Comparative genome analysis of Enterobacter cloacae. PLoS One 8:e74487. https://doi.org/10.1371/journal.pone.0074487
  17. MacFaddin, J. F. 2003. Biochemical tests for the identification of bacteria of clinical importance. Ed. Medica Panamericana, Buenos Aires, Argentina.
  18. Masyahit, M., Sijam, K., Awang, Y. and Ghazali, M. 2009. First report on bacterial soft rot disease on dragon fruit (Hylocereus spp.) caused by Enterobacter cloacae in peninsular Malaysia. Int. J. Agric. Biol. 11:659-666.
  19. Mezzatesta, M. L., Gona, F. and Stefani, S. 2012. Enterobacter cloacae complex: clinical impact and emerging antibiotic resistance. Future Microbiol. 7:887-902. https://doi.org/10.2217/fmb.12.61
  20. Miyoshi-Akiyama, T., Hayakawa, K., Ohmagari, N., Shimojima, M. and Kirikae, T. 2013. Multilocus sequence typing (MLST) for characterization of Enterobacter cloacae. PLoS One 8:e66358. https://doi.org/10.1371/journal.pone.0066358
  21. Murdoch, C. W. and Campana, R. J. 1983. Bacteria species associated with wetwood of elm. Phytopathology 73:1270-1273. https://doi.org/10.1094/Phyto-73-1270
  22. Needleman, S. B. and Wunsch, C. D. 1970. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48:443-453. https://doi.org/10.1016/0022-2836(70)90057-4
  23. Nishijima, K. A., Couey, H. M. and Alvarez, A. M. 1987. Internal yellowing, a bacterial disease of papaya fruits caused by Enterobacter cloacae. Plant Dis. 71:1029-1034. https://doi.org/10.1094/PD-71-1029
  24. Nishijima, K. A., Wall, M. M. and Siderhurst, M. S. 2007. Demonstrating pathogenicity of Enterobacter cloacae on macadamia and identifying associated volatiles of gray kernel of macadamia in Hawaii. Plant Dis. 91:1221-1228. https://doi.org/10.1094/PDIS-91-10-1221
  25. Paauw, A., Caspers, M. P. M., Schuren, F. H. J., Leverstein-van Hall, M. A., Deletoile, A., Montijn, R. C., Verhoef, J. and Fluit, A. C. 2008. Genomic diversity within the Enterobacter cloacae complex. PLoS One 3:e3018. https://doi.org/10.1371/journal.pone.0003018
  26. Rosen, H. R. 1922. The bacterial pathogen of corn stalk rot. Phytopathology 12:497-499.
  27. Sanders, J. W. and Sanders, C. C. 1997. Enterobacter spp.: pathogens poised to flourish at the turn of the century. Clin. Microbiol. Rev. 10:220-241.
  28. Santana, M. A., Rodriguez, M., Mathehus, J., Faks, J., Bocsanczy, A., Gerstl, A., Romay, G., Montilla, J., Fernande, C. E., Moreno-Zambrano, N. and Marval, D. 2012. A new bacterial disease of cassava in Venezuela caused by Enterobacter cloacae. Int. J. Agric. Biol. 14:183-189.
  29. Schroeder, B. K., Waters, T. D. and du Toit, L. J. 2010. Evaluation of onion cultivars for resistance to Enterobacter cloacae in storage. Plant Dis. 94:236-243. https://doi.org/10.1094/PDIS-94-2-0236
  30. Schroeder, B. K., DuToit, L. J. and Schwarts, H. F. 2009. First report of Enterobacter cloacae causing onion bulb rot in the Columbia Basin of Washington State. Plant Dis. 93:323.
  31. Takahashi, Y., Takahashi, K., Sato, M., Watanabe, K. and Kawano, T. 1997. Bacterial leaf rot of Odontioda orchids caused by Enterobacter cloacae. Ann. Phytopathol. Soc. Jpn. 63:164-169. https://doi.org/10.3186/jjphytopath.63.164
  32. Wang, G. F., Xie, G. L., Zhu, B., Huang, J. S., Liu, B., Kawicha, P., Benyon, L. and Duan, Y. P. 2010. Identification and characterization of Enterobacter complex causing mulberry (Morus alba) wilt disease in China. Eur. J. Plant Pathol. 126:465-478. https://doi.org/10.1007/s10658-009-9552-x
  33. Wick, R. L., Rane, K. K. and Sutton, D. K. 1987. Mung bean sprout disease caused by Enterobacter cloacae. Phytopathology 77:123.
  34. Zhang, Z. F. and Nan, Z. B. 2013. Occurrence of lucerne seedborne Enterobacter cloacae sprouts decay in Gansu Province of China. Eur. J. Plant Pathol. 135:5-9. https://doi.org/10.1007/s10658-012-0072-8