Assessment of antibacterial genes of emerging queen Apis mellifera L. induced by the bacterium Paenibacillus larvae larvae

Authors

  • SAS Gomaa Research and Training Centre on Vectors of Diseases, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt
  • EMS Barakat Department of Entomology, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt
  • MS Salama Department of Entomology, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt
  • EE El Gohary Research and Training Centre on Vectors of Diseases https://orcid.org/0000-0001-9607-3092

DOI:

https://doi.org/10.17159/2254-8854/2022/a13586

Keywords:

Honey-bee queen, American foulbrood, antimicrobial peptides, abacien, defensin, RT-PCR

Abstract

This study evaluated the expression of antimicrobial abaecin and defensin genes in virgin honey-bee queens (Apis mellifera) following induction of 4th larval instar with the bacterium Paenibacillus larvae larvae (1.07 × 102 CFU/queen); to investigate whether the presence of bacteria affects the immune response as well as gene transcript levels for the immune proteins. The total body proteins of bacteria-treated queens showed a highly significant increase, and the appearance of new proteins patterns and/or disappearance of others. The gene expression profile of treated queens showed up-regulation equalled four-fold of the defensin gene, whereas no progression occurred in the abacien gene. This finding likewise greatly affects the diseases challenging this pollinator.

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References

Aerts AM, Francois IE, Cammue BP, Thevissen K. 2008. The mode of antifungal action of plant, insect and human defensins. Cellular and Molecular Life Sciences 65(13): 2069–2079. https://doi.org/10.1007/s00018-008-8035-0

Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. 2001. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Critical Care Medicine 29(7): 1303–1310. https://doi.org/10.1097/00003246-200107000-00002

Antúnez K, Martín-Hernández R, Prieto L, Meana A, Zunino P, Higes M. 2009. Immune suppression in the honeybee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology Journal 11(9): 2284–2290. https://doi.org/10.1111/j.1462-2920.2009.01953.x

Auvynet C, Rosenstein Y. 2009. Multifunctional host defence peptides: antimicrobial peptides, the small yet big players in innate and adaptive immunity. The FEBS Journal. 276(22): 6497–6508. https://doi.org/10.1111/j.1742-4658.2009.07360.x

Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72(1-2): 248–254. https://doi.org/10.1016/0003-2697(76)90527-3

Cerda HP. 2003. Studies on resistance to Bacillus thuringiensis toxins in insects in relation to resistance management strategies. Ph.D. thesis, Biological Sciences, London University, London, U.K.

Choi YS, Choo YM, Lee KS, Yoon HJ, Kim I, Je YH, Sohn HD, Jin BR. 2008. Cloning and expression profiling of four antibacterial peptide genes from the bumblebee Bombus ignites. Comparative Biochemistry and Physiology B Biochemistry and Molecular Biology 150(2):141–146. https://doi.org/10.1016/j.cbpb.2008.02.007

Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D. Pettis JS, van Engelsdorp D, Evans JD. 2012. Pathogen webs in collapsing honey bee colonies. PLoS One 7(8): e43562. https://doi.org/10.1371/journal.pone.0043562

Compton SJ, Jones CG. 1985. Mechanism of dye response and interference in the Bradford protein assay. Analytical Biochemistry 151(2): 369–374. https://doi.org/10.1016/0003-2697(85)90190-3

Crailsheim K, Riessberger-Gallé U. 2001. Honey bee age-dependent resistance against American foulbrood. Apidologie 32: 91–103. https://doi.org/10.1051/apido:2001114

Cremer S, Armitage SAO, Schmid-Hempel P. 2007. Social immunity. Current Biology 17(16): R693–R702. https://doi.org/10.1016/j.cub.2007.06.008

Da Silva FP, Machado MC. 2012. Antimicrobial peptides: clinical relevance and therapeutic implications. Peptides 36(2): 308–314. https://doi.org/10.1016/j.peptides.2012.05.014

Danihlík J, Aronstein K, Petřivalský M. 2016. Antimicrobial peptides: a key component of honeybee innate immunity. Journal of Apicultural Research 54(2): 1–14.

Decanini L, Collins A, Evans J. 2007. Variation and heritability in immune gene expression by diseased honeybees. Journal of Heredity 98(3): 195–201. https://doi.org/10.1093/jhered/esm008

Doolittle GM. 1889. Scientific Queen-Rearing. Chicago, IL, U.S.A.: Thomas G. Newman & Son; 169 p.

Ekramoddoullah AKM, Davidson JJ. 1995. A method for the determination of conifer foliage protein extracted using sodium dodecyl sulphate and mercaptoethanol. Phytochemistry Analysis 6(1): 20–24.

Evans JD. 2004. Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. Journal of Invertebrate Pathology 85(2): 105–111. https://doi.org/10.1016/j.jip.2004.02.004

Evans JD. 2006. Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease. Journal of Invertebrate Pathology 93(2): 135–139. https://doi.org/10.1016/j.jip.2006.04.004

Evans JD, Lopez DL. 2004. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 97(3): 752–756. https://doi.org/10.1093/jee/97.3.752

Fries I, Martín R, Meana A, García-Palencia P, Higes M. 2006. Natural infections of Nosema ceranae in European honey bees. Journal of Apicultural Research 45(4): 230–233. https://doi.org/10.1080/00218839.2006.11101355

Genersch E, Forsgren E, Pentikäinen 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. International Journal of Systematic and Evolutionary Microbiology 56(3): 501–511. https://doi.org/10.1099/ijs.0.63928-0

Gomaa SAS. 2009. Characterization of the haemolymph of honey bee Apis mellifera (L.) following experimental infection with bacteria. M.Sc. thesis, Faculty of Science, Ain Shams University, Cairo, Egypt.

Gomaa S, El Gohary EE, Barakat E, Salama M. 2018. Morphometric analysis of some external and internal body characteristics of honey bee Apis mellifera queens treated with Paenibacillus larvae larvae. African Journal of Biological Sciences 14(1): 1–10. https://doi.org/10.21608/ajbs.2018.65271

Gomaa S, Barakat E, Salama M, El Gohary EE. 2021. Effect of the bacterium Paenibacillus larvae larvae on vitellogenin gene expression of the queen honey bee Apis mellifera L. African Entomology 29(1): 96–103. https://doi.org/10.4001/003.029.0096

Gomes PS, Fernandes MH. 2010. Defensins in the oral cavity: distribution and biological role. Journal of Oral Pathology & Medicine 39(1): 1–9. https://doi.org/10.1111/j.1600-0714.2009.00832.x

Green MR, Sambrook J. 2012. Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, New York, U.S.A.: CSHL Press. p. 631–1330.

Guaní-Guerra E, Santos-Mendoza T, Lugo-Reyes SO, Terán LM. 2010. Antimicrobial peptides: general overview and clinical implications in human health and disease. Clinical Immunology 135(1): 1–11. https://doi.org/10.1016/j.clim.2009.12.004

Hansen H, Brødsgaard CJ. 1999. American foulbrood: a review of its biology, diagnosis and control. Bee World 80(1): 5–23. https://doi.org/10.1080/0005772X.1999.11099415

Hasemann L. 1961. How long can spores of American foulbrood live? American Bee Journal 101:298–299.

Hatjina F, Bieńkowska M, Charistos L, Chlebo R, Costa C, Dražić MM, Filipi J, Gregorc A, Ivanova EN, Kezić N, et al. 2014. A review of methods used in some European countries for assessing the quality of honey bee queens through their physical characters and the performance of their colonies. Journal of Apicultural Research 53(3): 337–363. https://doi.org/10.3896/IBRA.1.53.3.02

Hoage TR, Rothenbuhler WC. 1966. Larval honey bee response to various doses of Bacillus larvaespores. Journal of Economic Entomology 59(1): 42–45. https://doi.org/10.1093/jee/59.1.42

HONEY BEE GENOME SEQUENCING CONSORTIUM. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443: 931–949. https://doi.org/10.1038/nature05260

Jarosz J. 1995. Haemolymph immune proteins protect the insect body cavity from invading bacteria. Comparative Biochemistry and Physiology 111: 213–220.

Kim SR, Lee EM, Yoon HJ, Choi YS, Yun EY, Hwang JS, Jin BR, Lee IH, Kim I. 2007. Antibacterial activity of peptides synthesized based on the Bombus ignites abaecin, a novel proline-rich antimicrobial peptide. International Journal of Industrial Entomology 14: 147–150.

Klaudiny J, Albert S, Bachanová K, Kopernicky J, Simúth J. 2005. Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. Insect Biochemistry and Molecular Biology 35(1): 11–22. https://doi.org/10.1016/j.ibmb.2004.09.007

Kwong WK, Mancenido AL, Moran NA. 2017. Immune system stimulation by the native gut microbiota of honey bees. Royal Society Open Science 4(2): 170003. https://doi.org/10.1098/rsos.170003

Kurtz J. 2004. Memory in the innate and adaptive immune systems. Microbes and Infection 6(15): 1410–1417. https://doi.org/10.1016/j.micinf.2004.10.002

Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259): 680–685. https://doi.org/10.1038/227680a0

Lapis K. 2008. Physiologic and pathophysiologic significance of antimicrobial (host defensive) small peptides. Orvosi Hetilap 51(149): 2419–2424. https://doi.org/10.1556/oh.2008.28511

Liyasove RA, Kutuev IA, Petukhov AV, Poskryakov AV, Nikolenko AG. 2011. Phylogenetic relationships of dark European honeybees Apis mellifera mellifera L. from the Russian Ural and West European populations. Journal of the Apicultural Science 55(1): 67–76.

Lopez J, Moreno G, Sancristobal I, Murua J. 2014. Transgenerational immune priming in honeybees. Proceedings of the Royal Society B: Biological Sciences 281: 0454.

Randolt K, Gimple O, Geissendorfer J, Reinders J, Prusko C, Mueller JM, Albert S, Tautz J, Beier H. 2008. Immune-rrelated proteins induced in the hemolymph after aseptic and septic injury differ in honey bee worker larvae and adults. Archive of Insect Biochemistry and Physiology 69(4): 155–167. https://doi.org/10.1002/arch.20269

Rowley AF, Powell A. 2007, Invertebrate immune systems – specific, quasi-specific, or nonspecific? Journal of Immunology 179(11):7 209–7214. https://doi.org/10.4049/jimmunol.179.11.7209

Schmid-Hempel P. 1998. Parasites in Socal Insects. Princeton, NJ, U.S.A.: Princeton University Press.

Sedmak JJ, Grossberg SE. 1977. A rapid, sensitive and versatile assay for protein using Coomassie Brilliant Blue G-250. Analytical Biochemistry. 79(1-2): 544–552. https://doi.org/10.1016/0003-2697(77)90428-6

Teixeira V, Feio MJ, Bastos M. 2012. Role of lipids in the interaction of antimicrobial peptides with membranes. Progress in Lipid Research 51(2): 149–177. https://doi.org/10.1016/j.plipres.2011.12.005

Tzou PF, Reichhart J-M, Lemaitre B. 2002. Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants. Proceedings of the National Academy of Science USA 99(4): 2152–2157. https://doi.org/10.1073/pnas.042411999

Werner T, Liu G, Kang D, Ekengren S, Steiner H, Hultmark D. 2000. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster Proceedings of the National Academy of Science USA 97(25): 13772–13777. https://doi.org/10.1073/pnas.97.25.13772

Xu P, Shi M, Chen X. 2009. Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. PLoS One 4(1): e4239. https://doi.org/10.1371/journal.pone.0004239

Yuan GC, Ma P, Zhong W, Liu JS. 2006. Statistical assessment of the global regulatory role of histone acetylation in Saccharomyces cerevisiae. Genome Biology 7(8): R70. https://doi.org/10.1186/gb-2006-7-8-r70

Yue D, Nordhoff M, Wieler LH, Genersch E. 2008, Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environental Microbiology 10(6): 1612–1620. https://doi.org/10.1111/j.1462-2920.2008.01579.x

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Published

2022-09-19

How to Cite

1.
Gomaa S, Barakat E, Salama M, El Gohary E. Assessment of antibacterial genes of emerging queen Apis mellifera L. induced by the bacterium Paenibacillus larvae larvae. Afr. Entomol. [Internet]. 2022 Sep. 19 [cited 2024 Apr. 20];30. Available from: https://www.africanentomology.com/article/view/13586

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