Typing of Pantoea agglomerans isolated from colonies of honey bees (Apis mellifera) and culturability of selected strains from honey

Apidologie

Volumn 40, Issue 1, 2009, Pages 40-54

  Loncaric, Igor ^a,b   Heigl, Helmut ^b   Licek, Elisabeth ^a   Moosbeckhofer, Rudolf ^b   Busse, Hans Jürgen ^a   Rosengarten, Renate ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b AUSTRIAN AGENCY FOR HEALTH AND FOOD SAFETY   (Austria)

Author keywords

Bacterial diversity; Erwinia amylovora; Genomic fingerprinting; Pollen analysis; Strain traceability

Indexed keywords

BACTERIAL DISEASE; BACTERIUM; BIOCONTROL AGENT; DNA FINGERPRINTING; GENOMICS; HONEYBEE; INOCULATION; ISOLATED POPULATION; NECTAR; PALYNOLOGY;

APIS MELLIFERA; BACTERIA (MICROORGANISMS); CUCUMIS MELO VAR. INODORUS; ERWINIA AMYLOVORA; PANTOEA AGGLOMERANS;

EID: 60749092312     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1051/apido/2008062     Document Type: Article

References (68)

1. Alexandrova M., Porrini C., Bazzi C., Carpana E., Bigliardi M., Sabatini A.G. (2002) Erwinia amylovora longevity in beehives, beehive products and honeybees, Acta Hortic. (ISHS) 590, 201-205.
2. Bakonyi T., Derakhshifar I., Grabensteiner E., Nowotny N. (2003) Development and evaluation of PCR assays for the detection of Paenibacillus larvae in honey samples: comparison with isolation and biochemical characterization, Appl. Environ. Microbiol. 69, 1504-1510.
3. Beyme D., Ficke W., Kleinhempel H., Schaefe, H.J., Bremer R. (1975) Modellversuche zur Überlebensdauer von Erwinia amylovora im Verdauungstrakt der Honigbiene, im Honig und an Teilen des Bienenstockes, Arch. Phytopathol. u. Pflanzenschutz 11, 203-211.
4. Cicchetti R., Iacobini M., Midolla F., Papoff P., Mancuso M., Moretti C. (2006) Pantoea agglomerans sepsis after rotavirus gastroenteritis, Pediatr. Infect. Dis J. 25, 280-281.
5. Costa E., Usall J., Teixido N., Delgado J., Vinas I. (2002) Water activity, temperature, and pH effects on growth of the biocontrol agent Pantoea agglomerans CPA-2, Can. J. Microbiol. 4, 1082-1088.
6. Cruz A.T., Cazacu A.C., Allen C.H. (2007) Pantoea agglomerans - a plant pathogen causing human disease, J. Clin. Microbiol. 45, 1989-1992.
7. de Vos P. (2002) Nucleic acid analysis and SDSPAGE of whole-cell proteins in Bacillus taxonomy, in: Berkeley R., Heyndrickx M., Logan N., de Vos P. (Eds.), Applications and systematics of Bacillus and relatives, Blackwell Publishing, Oxford, pp. 141-159.
8. de Wael L., Greef M., Laere O. (1990) The honeybees as a possible vector of Erwinia amylovora (Burr.) Winslow et al., Acta Hortic. (ISHS) 273, 107-114.
9. Dutkiewicz J. (1997) Bacteria and fungi in organic dust as potential health hazard, Ann Agric. Environ. Med. 4, 11-16.
10. Esteban J., Molleja A., Cabria F., Soledad Jimenez M. (2003) SDS-PAGE for identification of species belonging to the Mycobacterium fortuitum complex, Clin. Microbiol. Infect. 9, 327-331.
11. Garcia-Vallvé S., Palau J., Romeu A. (1999) Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis, Mol. Biol. Evol. 16, 1125-1134.
12. Gavini F., Mergaert J., Beji A., Mielcarek C., Izard D., Kersters K., De Ley J. (1989) Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and description of Pantoea dispersa sp. nov., Int. J. Syst. Bacteriol. 39, 337-345.
13. Genersch E., Forsgren E., Pentikainen J., Ashiralieva A., Rauch S., Kilwinski J., Fries I. (2006) Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation, Int. J. Syst. Evol. Microbiol. 56, 501-511.
14. Gerhard P., Murray R.E., Wood W.A., Krieg R. (1994) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC.
15. Gilliam M. (1997) Identification and roles of nonpathogenic microflora associated with honey bees, FEMS Microbiol. Lett. 155, 1-10.
16. Heck K.L. Jr., Van Belle G., Simberloff D. (1975) Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size, Ecology 56, 1459-1461.
17. Heissenberger B. (2004) Untersuchungen zur biologischen Feuerbrandbekämpfung mit Pantoea agglomerans, einer erregerverwandten Bakterienart. Diploma thesis, University of Natural Resources and Applied Life Sciences, Vienna, Austria.
18. Heissenberger B., Spornberger A., Loncaric I., Moosbeckhofer R., Keck M., Foissy H. (2006) In vitro studies on fire blight control by bacterial antagonists, Proc. 1st Int. Symp. on Biological Control of Bacterial Plant Diseases, in: Zeller W., Ulrich C. (Eds.), Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft Berlin-Dahlem 408, pp. 281-282.
19. Holland S.M. (2003). Analytic rarefaction, version 1.3. University of Georgia, Athens, [online] http://www.uga.edu/strata/software/Software.html (accessed on 9 October 2008).
20. Horn H. (1992) Das grosse Honigbuch: Entstehung, Gewinnung, Zusammensetzung, Qualität, Gesundheit und Vermarktung, Ehrenwirth Verlag, München.
21. Hurlbert S.H. (1971). The nonconcept of species diversity: a critique and alternative parameters, Ecology 52, 577-586.
22. Ishimaru C.A., Klos E.J., Brubaker R.R. (1988) Multiple antibiotic production by Erwinia herbicola, Phytopathology 78, 746-750.
23. Jeyaprakash A., Hoy M.A., Allsopp M.H. (2003) Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences, J. Invertebr. Pathol. 84, 96-103.
24. Kardos G., Nagy J., Antal M., Bistyak A., Tenk M., Kiss I. (2007) Development of a novel PCR assay specific for Riemerella anatipestifer, Lett. Appl. Microbiol. 44, 145-148.
25. Kearns L.P., Hale C.N. (1996) Partial characterization of an inhibitory strain of Erwinia herbicola with potential as a biocontrol agent for Erwinia amylovora, the fire blight pathogen, J. Appl. Bacteriol. 81, 369-374.
26. Koo H.S., Kim J.S., Eom J.S., You J.Y., Park J.Y., Kim H.S., Song W., Cho H.C., Lee K.M. (2006) Pseudooutbreak of Pantoea species bacteremia associated with contaminated cotton pledgets, Am. J. Infect. Control 34, 443-446.
27. 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.
28. Krell R. (1996) Value-added products from beekeeping: Physical characteristics of honey, FAO Agricultural services bulletin No. 124, Rome, [online] http://www.fao.org/docrep/w0076e/w0076e00.htm#con (accessed on 9 October 2008).
29. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 15, 227, 680-685.
30. Laporte C., Demachy M.C., Thevenin-Lemoine C. (2002) Ostéite tibiale à Pantoea agglomerans au décours d'une fracture ouverte stade IIIB de jambe, Rev. Chir. Orthop. Réparatrice Appar. Mot. 88, 625-627.
31. Lau K.K., Ault B.H., Jones D.P. (2005) Polymicrobial peritonitis including Pantoea agglomerans from teething on a catheter, South.Med. J. 98, 580-581.
32. Lim P.S., Chen S.L., Tsai C.Y., Pai M.A. (2006) Pantoea peritonitis in a patient receiving chronic ambulatory peritoneal dialysis, Nephrology (Carlton) 11, 97-99.
33. Loncaric I., Donat C., Antlinger B., Oberlerchner J.T., Heissenberger B., Moosbeckhofer R. (2008) Strain-specific detection of two Aureobasidium pullulans strains, fungal biocontrol agents of fire blight by new, developed multiplex-PCR, J. Appl. Microbiol. 104, 1433-1441.
34. Louveaux J., Maurizio A., Vorwohl G. (1970) Internationale Kommission für Bienenbotanik der I.U.B.S. - Methodik der Melissopalynologie, Apidologie 1, 193-209; English version in Bee World, 1970, 51, 125-138.
35. Lyra C., Hantula J., Vainio E., Rapala J., Rouhiainen L., Sivonen K. (1997) Characterization of cyanobacteria by SDS-PAGE of whole-cell proteins and PCR/RFLP of the 16S rRNA gene, Arch. Microbiol. 168, 176-184.
36. Mbwana J., Bolin I., Lyamuya E., Mhalu F., Lagergard T. (2006) Molecular characterization of Haemophilus ducreyi isolates from different geographical locations, J. Clin. Microbiol. 44, 132-137.
37. Mohr K.I., Tebbe C.C. (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field, Environ. Microbiol. 8, 258-272.
38. Mohr K.I., Tebbe C.C. (2007) Field study results on the probability and risk of a horizontal gene transfer from transgenic herbicide-resistant oilseed rape pollen to gut bacteria of bees, Appl. Microbiol. Biotechnol. 75, 573-582.
39. Molan P.C. (1992a) The antibacterial activity of honey: 1. The nature of the antibacterial activity, Bee World 73, 5-28.
40. Molan P.C. (1992b) The antibacterial activity of honey: 2. Variation in the potency of the antibacterial activity, Bee World 73, 59-76.
41. Nuclo R.L., Johnson K.B., Sugar D., Stockwell V.O. (1998) Secondary colonization of pear blossoms by two bacterial antagonists of the fire blight pathogen, Plant Dis. 82, 661-668.
42. Ordax M., Marco-Noalesm E., Lopez M.M., Biosca E.G. (2006) Survival strategy of Erwinia amylovora against copper: induction of the viable-but-nonculturable state, Appl. Environ. Microbiol. 72, 3482-3488.
43. Özaktan H., Bora T. (2004) Biological control of fire blight in pear orchards with a formulation of Pantoea agglomerans strain Eh 24, Braz. J. Microbiol. 35, 224-229.
44. Page R.D.M. (1996) TREEVIEW: An application to display phylogenetic trees on personal computers, Comp. Appl. Biosci. 12, 357-358.
45. PONET- pollen database, Institute for Apiculture, Austrian Agency for Health and Food Safety, [online] http://www15.ages.at:7778/pls/pollen/pollen- suche (accessed on 9 October 2008).
46. Pot B., Vandamme P., Kersters K. (1994) Analysis of electrophoretic whole-organism protein fingerprints, in: Goodfellow M., O'Donnell A.G. (Eds.), Modern microbiological methods, Chemical methods in prokaryotic systematic, Chichester, England, John Wiley and Sons, pp. 493-521.
47. Pusey P.L. (1997) Crab apple blossoms as a model system for fire blight biocontrol research, Phytopathology 87, 1096-1102.
48. Rada V., Machoa M., Huk J., Marounek M., Duskova D. (1997) Microflora in the honeybee digestive tract: counts, characteristics and sensitivity to veterinary drugs, Apidologie 28, 357-365.
49. Rall V.L., Bombo A.J., Lopes T.F., Carvalho L.R., Silva M.G. (2003) Honey consumption in the state of Sao Paulo: a risk to human health? Anaerobe 9, 299-303.
50. Ravenschlag K., Sahm K., Pernthaler J., Amann R. (1999) High bacterial diversity in permanently cold marine sediments, Appl. Environ. Microbiol. 65, 3982-3989.
51. Ritter W. (1982) Experimenteller Beitrag zur Thermoregulation des Bienenvolks (Apis mellifera L.), Apidologie 13, 169-195.
52. Seeley T.D. (1997) Honigbienen - Im Mikrokosmos des Bienenstocks, Birkhäuser Verlag, Basel.
53. Sneath P.H.A., Sokal R.R. (1973) Numerical Taxonomy, W.H. & Freeman, San Francisco.
54. Snowdon J.A., Cliver D.O. (1996) Microorganisms in honey, Int. J. Food Microbiol. 31, 1-26.
55. Southwick E.E. (1991) The colony as a thermoregulating superorganism, in: Goodman L.J., Fisher R.C. (Eds.), The behavior and physiology of bees, CAB International, Oxon, UK, pp. 28-47.
56. Tysset C., Durand C. (1973) On the survival of some gram negative, non-sporulated bacteria in commercial honey, Bull. Acad. Vet. Fr. 46, 191-196.
57. Tysset C., Haas P., Durand C. (1979) Survival of some mycobacteria in honey stored at room temperature, Bull. Acad. Vet. Fr. 52, 447-452.
58. Vanneste J.L. (1996) Honey bees and epiphytic bacteria to control fire blight, a bacterial disease of apple and pears, Biocontrol News Inform. 17, 67N-78N.
59. Vanneste J.L., Cornish D.A., Yu J., Voyle M.D. (2002) P10C: a new biological control agent for control of fire blight which can be sprayed or distributed using honey bees, Acta Hortic. (ISHS) 590, 231-235.
60. Vanneste J.L., Yu J., Beer S.V. (1992) Role of antibiotic production by Erwinia herbicola Eh252 in biological control of Erwinia amylovora, J. Bacteriol. 174, 2785-2796.
61. Versalovic J., Koeuth T., Lupski J.R. (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes, Nucleic Acids Res. 19, 6823-6831.
62. Wieser M., Busse H.J. (2000) Rapid identification of Staphylococcus epidermidis, Int. J. Syst. Evol. Microbiol. 50, 1087-1093.
63. Williams J.G., Kubelik A.R., Livak K.J., Rafalski J.A., Tingey S.V. (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers, Nucleic Acids Res. 18, 6531-6535.
64. Wilson M., Epton H.A.S., Sigee D.C. (1990) Biological control of fire blight of hawthorn (Crategus monogyna) with Erwinia herbicola under protected conditions, Plant Pathol. 39, 301-308.
65. Wodzinski R.S., Umholtz T.E., Rundle J.R., Beer S.V. (1994) Mechanisms of inhibition of Erwinia amylovora by E. herbicola in vitro and in vivo, J. Appl. Bacteriol. 76, 22-29.
66. Wright S.A.I., Beer S.V. (1996) The role of antibiotics in biological control of fire blight by Erwinia herbicola strain EH318, Acta Hortic. (ISHS) 411, 309-312.
67. Wright S.A.I., Beer S.V. (2006) Pantoea agglomerans, a biocontrol agent and ubiquitous microorganism - friend or foe? Proc. 1st Int. Symp. on Biological Control of Bacterial Plant Diseases, in: Zeller W., Ulrich C. (Eds.), Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft Berlin-Dahlem, 408, pp. 334-338.
68. Wright S.A., Zumoff C.H., Schneider L., Beer S.V. (2001) Pantoea agglomerans strain EH318 produces two antibiotics that inhibit Erwinia amylovora in vitro, Appl. Environ. Microbiol. 67, 284-292.