Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Journal of Apicultural Science

The Journal of Research Institute of Horticulture and Apicultural Research Association

2 Issues per year


IMPACT FACTOR 2016: 0.722
5-year IMPACT FACTOR: 0.944

CiteScore 2016: 0.84

SCImago Journal Rank (SJR) 2016: 0.414
Source Normalized Impact per Paper (SNIP) 2016: 0.616

Open Access
Online
ISSN
2299-4831
See all formats and pricing
Online
Open Access
*Prices in US$ apply to orders placed in the Americas only. Prices in GBP apply to orders placed in Great Britain only. Prices in € represent the retail prices valid in Germany (unless otherwise indicated). Prices are subject to change without notice. Prices do not include postage and handling if applicable. RRP: Recommended Retail Price.
More options …
Volume 58, Issue 1
Loading journal volume and issue information...

Antagonistic Effect of Gut Bacteria in the Hybrid Carniolan Honey Bee, Apis Mellifera Carnica, Against Ascosphaera Apis, the Causal Organism of Chalkbrood Disease

Mohamed O. M. Omar
  • Chair of Engineer Abdullah Baqshan for Bee Research, Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, PO Box 2460, KSA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Adhm M. Moustafa / Mohammad J. Ansari
  • Corresponding author
  • Chair of Engineer Abdullah Baqshan for Bee Research, Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, PO Box 2460, KSA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Abdelsalam M. Anwar
  • Chair of Engineer Abdullah Baqshan for Bee Research, Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, PO Box 2460, KSA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Bassam F. Fahmy / Ahmad Al-Ghamdi
  • Chair of Engineer Abdullah Baqshan for Bee Research, Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, PO Box 2460, KSA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
 / Adgaba Nuru
  • Chair of Engineer Abdullah Baqshan for Bee Research, Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, PO Box 2460, KSA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2014-05-27 | DOI: https://doi.org/10.2478/jas-2014-0002

Open Access

Download PDF

Abstract

The objective of this study was to isolate and characterize bacterial strains associated with the gut of the hybrid Carniolan honey bee, Apis mellifera carnica, and to determine their in vitro and in vivo potential against Ascosphaera apis, the causal organism of chalkbrood disease, with the purpose of exploring feasible biological control. Six bacterial strains were isolated from healthy worker honey bees by culture-dependent methods. Six fungal strains (A3, A4, A7, A8, A9, and A15) of A. apis were isolated from larvae suffering from chalkbrood disease on Yeast-Glucose-Starch agar (YGPSA) medium. All bacteria were identified by a combination of morphology, Gram stain, and 16S rRNA sequence analysis, and fungal strains were identified by morphology and 5.8S rRNA. In vitro and in vivo inhibition assays were carried out to determine the ability of bacterial isolates to inhibit A. apis, the causal agent of chalkbrood disease. The analysis of 16S rRNA sequences revealed that four bacterial strains (B2, B4, B10, and B100) belong to Bacillus subtilis species, and two strains (P1 and P5) belong to Pseudomonas fluorescence. Significant differences in antagonistic activity of all bacterial strains were observed. B. subtilis isolate B2 showed the highest antagonistic activity, as measured by the inhibition zone against A. apis, followed by the P1 strain of P. fluorescence. SEM analysis also supports the antagonistic activity of these bacteria against A. apis. This study provides a theoretical basis for biological control of honey bee chalkbrood disease.

Keywords: antifungal activity; Apis mellifera carnica; Ascosphaera apis; growth inhibition assay; gut bacteria; scanning electron microscopy

References

  • Anderson D. L., Gibson N. L. (1998) New species and isolate of sporecysts fungi (Plectomycetes: Ascosphaerales) from Australia. Australian Systematic Botany 11: 53-72.CrossrefGoogle Scholar

  • Aronstein K. A., Murray K. D. (2010) Chalkbrood disease in honey bees. Journal of Invertebrate Pathology 103: 520-529.Web of ScienceGoogle Scholar

  • Aronstein K. A., Murray K. D., de Leon J., Qin X., Weinstock G. (2007) High mobility group (HMG-box) genes in the honey bee fungal pathogen Ascosphaera apis. Mycologia 99 (4): 553-561.CrossrefWeb of ScienceGoogle Scholar

  • Azambuja P., Garcia E. S., Ratcliffe N. A. (2005) Gut microbiota and parasite transmission by insect vectors. Trends in Parasitology 21: 568-572.PubMedCrossrefGoogle Scholar

  • Bailey L., Ball B. V. (1991) Honey Bee Pathology. Academic Press London, UK. 193 pp.Google Scholar

  • Bissett J. D., Duke G. M., Goettel M. S. (1996) Ascosphaera acerosa sp. nov. isolated from the alfalfa leaf cutting bee, with a key to the species of Ascosphaera. Mycologia 88: 797-803.CrossrefGoogle Scholar

  • Breed R. S., Murray E. G. D., Smith N. R. (1957) Bergey’s Manual of Determinative Bacteriology. Williams Wilkins Company. Baltimore, Maryland. 1094 pp.Google Scholar

  • Chen Y., Evans J. D., Smith I. B., Pettis J. S. (2008) Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology 97: 186-188.CrossrefPubMedWeb of ScienceGoogle Scholar

  • Chorbiński P. (2003) Wrażliwość szczepów Ascosphaera apis na preparaty przeciwgrzybicze. Medycyna Weterynaryjna 59 (12): 1137-1139.Google Scholar

  • Cox-Foster D. L., Conlan S., Holmes E. C., Palacios G., Evans J. D., Moran N. A., Quan P. L., Briese T., Hornig M., Geiser D. M., Martinson V., Van-Engelsdorp D., Kalkstein A. L., Drysdale A., Hui J., Zhai J., Cui L., Hutchinson S. K., Simons J. F., Egolm M., Pettis J. S., Lipkin W. I. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287.Web of ScienceGoogle Scholar

  • Davis C., Ward W. (2003) Control of chalkbrood disease with natural products: a report for the RIRDC. Publication No. 03/107. Kingston, ACT, AU. 23 pp.Google Scholar

  • Evans J. D., Armstrong T. N. (2006) Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecology 6: 4-12.CrossrefPubMedGoogle Scholar

  • Evans J. D., Lopez D. L. (2004) Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 97: 752-756.CrossrefPubMedGoogle Scholar

  • Flores J., Spivak M., Gutierrez I. (2005) Spores of Ascosphaera apis contained in wax foundation can infect honey bee brood. Veterinary Microbiology 108: 141-144.CrossrefGoogle Scholar

  • Foldes T., Banhegyi I., Herpai Z., Varga L., Szigeti J. (2000) Isolation of Bacillus strains from the rhizosphere of cereals and in vitro screening for antagonism against phytopathogenic, food-borne pathogenic and spoilage micro-organisms. Journal of Applied Microbiology 89: 840-846.CrossrefPubMedGoogle Scholar

  • Frazier M., Mullin C., Frazier J., Ashcraft S. (2008) What have pesticides got to do with it? American Bee Journal 148: 521-523.Google Scholar

  • Gallai N., Salles J., Settele J., Vaissière B. E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810-21.Web of ScienceGoogle Scholar

  • Gilliam M. (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiology Letters 155: 1-10.Google Scholar

  • Gliński Z., Chmielewski M. (1996) Imidazole derivatives in control of the honey bee brood mycoses. Pszczelnicze Zeszyty Naukowe 40 (2): 165-173.Google Scholar

  • Heath L. A. F. (1982) Development of chalk brood in a honey bee colony; chalk brood pathogens: a review. Bee World 63 (3): 119-135.Google Scholar

  • Hornitzky M. (2001) Literature review of chalkbrood. A report for the RIRDC. Publication No. 01/150. Kingston, ACT, AU. 17pp.Google Scholar

  • Indiragandhi P., Anandham R., Madhaiyan M., Poonguzhali S., Kim G. H., Saravanan V. S., Sa T. (2007) Cultivable bacteria associated with larval gut of prothiofos-resistant, prothiofos-susceptible and field-caught populations of diamondback moth, Plutella xylostella and their potential for antagonism towards entomopathogenic fungi and host insect nutrition. Journal of Applied Microbiology 103: 2664-2675.Web of ScienceGoogle Scholar

  • James R. R., Skinner J. S. (2005) PCR diagnostic methods for Ascosphaera infections in bees. Journal of Invertebrate Pathology 90 (2): 98-103. CrossrefPubMedGoogle Scholar

  • Jeyaprakash A. M., Hoy 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. Journal of Invertebrate Pathology 84: 96-103.Google Scholar

  • Kaur R., Macleod J., Foley W., Nayudu M. (2006) Gluconic Acid: An Antifungal Agent Produced by Pseudomonas Species in Biological Control of Take-All. Photochemistry 67(6): 595-604.CrossrefGoogle Scholar

  • Li J., Zheng Z., Hong S., Qi X., Liang Q. (2012) Isolation and Identification of an Antagonistic Bacterial Strain Against Ascosphaera apis from Honey bee Larvae Infected with Chalkbrood Disease. Scientia Agricultural Sinica (5): 5-20. DOI: CNKI:SUN:ZNYK.0.2012-05-020Google Scholar

  • Liu T. P. (1991) Ultrastructural changes in the spore and mycelia of Ascosphaera apis after treatment with benomyl (Benlate 50 W). Mycopathologia 116: 23-28.Google Scholar

  • 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. Environmental Microbiology 8: 258-272.PubMedCrossrefGoogle Scholar

  • Nayudu M., Khan S. (2009) Biological Control of Chalkbrood by Anti-fungal Bacterial Symbionts of Bees. A report for the RIRDC. Publication No. 09/120. Kingston, ACT, AU. 14 pp.Google Scholar

  • Nelson D. L., Gochnauer T. A. (1982) Field and laboratory studies on chalkbrood disease of honey bees. American Bee Journal 122: 29-34.Google Scholar

  • Pattabhiramaiah M., Reddy M. S., Brueckner D. (2012) Detection of novel probiotic bacterium Lactobacillus spp. in the workers of Indian honey bee, Apis cerana indica. International Journal of Environmental Science 2(3): 1135-1143.Google Scholar

  • Romero-Tabarez M., Jansen R., Sylla M., Lünsdorf H., Häussler S., Santosa D. A., Timmis K. N., Molinari G. (2006) 7-Omalonyl macrolactin A, a new macrolactin antibiotic from Bacillus subtilis active against methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, and a small-colony variant of Burkholderia cepacia. Antimicrobial Agents and Chemotherapy 50: 1701-1709.Google Scholar

  • Sabaté D. C., Carrillo L., Audisio M. C. (2009) Inhibition of Paenibacillus larvae and Ascophaera apis by Bacillus subtilis isolated from honey bee gut and honey samples. Research in Microbiology 160: 193-199.Web of ScienceGoogle Scholar

  • Spiltoir C. F. (1955) Life cycle of Ascosphaera apis (Pericystis apis). American Journal of Botany 42: 501-508.Google Scholar

  • Theantana T., Chantawannakul P. (2008) Protease and ß-N acetylglucosaminidase of honey bee chalkbrood pathogen Ascosphaera apis. Journal of Apicultural Research 47 (1): 68-76. van Engelsdorp D., Meixner M. D. (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology 103: 80-95.Google Scholar

  • Yoshiyama M., Kimura K. (2009) Bacteria in the gut of Japanese honey bee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. Journal of Invertebrate Pathology 102: 91-96.CrossrefWeb of ScienceGoogle Scholar

  • Zaghloul O. A., Mourad A. K, El-Kady M. B., Nemat F. M., Morsy M. E. (2005) Assessment of losses in honey yield due to the chalk brood disease, with reference to the determination of its economic injury levels in Egypt. Communications in Agricultural and Applied Biological Sciences 70(4): 703-714. Google Scholar

About the article

Received: 2012-12-25

Accepted: 2014-04-11

Published Online: 2014-05-27

Published in Print: 2014-06-01

Citation Information: Journal of Apicultural Science, Volume 58, Issue 1, Pages 17–27, ISSN (Online) 2299-4831, DOI: https://doi.org/10.2478/jas-2014-0002.

Export Citation

© by Mohammad J. Ansari. This article is distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Gil Leclercq, Bart Pannebakker, Nicolas Gengler, Bach Kim Nguyen, and Frédéric Francis
Journal of Apicultural Research, 2017, Volume 56, Number 4, Page 366
[2]
Simona Nardoni, Carlo D’Ascenzi, Guido Rocchigiani, Roberto Amerigo Papini, Luisa Pistelli, Giovanni Formato, Basma Najar, and Francesca Mancianti
Natural Product Research, 2017, Page 1
[3]
Sophie EF Evison
Current Opinion in Insect Science, 2015, Volume 10, Page 65

Comments (0)

Please log in or register to comment.
Log in