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Supplementation with an Inorganic Iron Source Modulates the Metalloproteomic Profile of the Royal Jelly Produced by Apis mellifera L.

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Abstract

This study aimed to evaluate the quality of the royal jelly produced by Apis mellifera bees in the presence of different iron concentrations (ferrous sulfate heptahydrate—0, 25, 50, and 100 mg L−1). Two-dimensional electrophoresis was used for the fractionation of royal jelly proteins, and iron level was quantified using flame atomic absorption spectrometry technique. The proteins were identified using electrospray ionisation mass spectrometry. Analysis of variance followed by the Tukey test (P < 0.05) was utilised. Dietary supplementation with mineral Fe affected the protein content and number of proteins in the experimental period. Further, the diet containing the highest iron concentration showed a greater number of spots containing iron, as well as in the abdomen of the bees. The most protein containing Fe were classified as major royal jelly proteins. These results showed that Fe influenced the quality of royal jelly and can improve its nutritional value.

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References

  1. Li P, Yin Y-L, Li D, Woo Kim S, Wu G (2007) Amino acids and immune function. Br J Nutr 98(2):237. https://doi.org/10.1017/S000711450769936X

    Article  CAS  PubMed  Google Scholar 

  2. Haraguchi H (2004) Metallomics as integrated biometal science. J Anal At Spectrom 19(1):5. https://doi.org/10.1039/b308213j

    Article  CAS  Google Scholar 

  3. Nichol H, Law JH, Winzerling JJ (2002) Iron metabolism in insects. Annu Rev Entomol 47(1):535–559. https://doi.org/10.1146/annurev.ento.47.091201.145237

    Article  CAS  PubMed  Google Scholar 

  4. Crabtree B, Newsholme EA (1972) Comparative aspects of fuel utilization and metabolism by muscle. Insect Muscle (ed P N R Usherwood):405–500

  5. Manning R (2016) Artificial feeding of honeybees based on an understanding of nutritional principles. Anim Prod Sci 58(4):689. https://doi.org/10.1071/AN15814

    Article  Google Scholar 

  6. Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41(3):278–294. https://doi.org/10.1051/apido/2010012

    Article  Google Scholar 

  7. Deseyn J, Billen J (2005) Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae). Apidologie 36(1):49–57. https://doi.org/10.1051/apido:2004068

    Article  Google Scholar 

  8. Coelho MS, Silva JH, Oliveira JHV, Oliviera ERA, Araújo JA, Lima MR (2008) Alimentos convencionais e alternativos para abelhas. Caatinga, v. 21, n. 1, pp 1–9

    Google Scholar 

  9. Wang D (1965) Growth rates of young queen and worker-honeybee larvae. J Apic Res, v 4:3–5

    Article  Google Scholar 

  10. Alves MLTMF (2012) Avaliação do potencial antioxidante da geleia real ao longo do tempo de armazenamento. Biotemas 25(3):257–263. https://doi.org/10.5007/2175-7925.2012v25n3p257

    Article  Google Scholar 

  11. Carvalheira JBC, Zecchin HG, Saad MJA (2002) Vias de Sinalização da Insulina. Arq Bras Endocrinol Metabol 46(4):419–425. https://doi.org/10.1590/S0004-27302002000400013

    Article  Google Scholar 

  12. www.uniprot.org (2018) UniProt. Retirado 18 de maio de 2018, de http://www.uniprot.org/. Accessed 20 Apr 2018

  13. Braga CP, Bittarello AC, Padilha CCF, Leite AL, Moraes PM, Buzalaf MAR, Zara LF, Padilha PM (2015) Mercury fractionation in dourada (Brachyplatystoma rousseauxii) of the Madeira River in Brazil using metalloproteomic strategies. Talanta 132:239–244. https://doi.org/10.1016/J.TALANTA.2014.09.021

    Article  CAS  PubMed  Google Scholar 

  14. Sun Y, An S, Henrich VC, Xiaoping Sun A, & Song Q (2007) Proteomic identification of PKC-mediated expression of 20E-induced protein in Drosophila melanogaster. https://doi.org/10.1021/PR0705183

  15. Xiao-Fan Zhao, H.-J. He, Du-Juan Dong, & Wang, J.-X. (2005). Identification of differentially expressed proteins during larval molting of Helicoverpa armigera. 10.1021/PR0502424

  16. Zhang G, Zhang W, Cui X, Xu B (2015) Zinc nutrition increases the antioxidant defenses of honey bees. Entomol Exp Appl 156(3):201–210. https://doi.org/10.1111/eea.12342

    Article  CAS  Google Scholar 

  17. Herbert EW Jr, Shimanuki H (1978) Mineral requirements for brood-rearing by honeybees fed a synthetic diet. J Apic Res 17(3):118–122

    Article  CAS  Google Scholar 

  18. Doolittle GMM (1899) Doolittle ́s queen rearing methods. Am Bee J 39(28):435–436

    Google Scholar 

  19. Vieira JCS, Cavecci B, Queiroz JV, Braga CP, Padilha CCF, Leite AL, Figueiredo WS, Buzalaf MAR, Zara LF, Padilha PM (2015) Determination of the mercury fraction linked to protein of muscle and liver tissue of Tucunaré (Cichla spp.) from the Amazon Region of Brazil. Arch Environ Contam Toxicol 69(4):422–430. https://doi.org/10.1007/s00244-015-0160-9

    Article  CAS  PubMed  Google Scholar 

  20. dos Santos FA, Cavecci B, Vieira JCS, Franzini VP, Santos A, de Lima Leite A, Buzalaf MAR, de Zara LF, Magalhães Padilha P (2015) A metalloproteomics study on the association of mercury with breast milk in samples from lactating women in the Amazon Region of Brazil. Arch Environ Contam Toxicol 69(2):223–229. https://doi.org/10.1007/s00244-015-0161-8

    Article  CAS  PubMed  Google Scholar 

  21. Lima, P. M., Neves, R. D. C. F., dos Santos, F. A, Pérez, C. A, da Silva, M. O. A, Arruda, M. A Z., … Padilha, P. M. (2010). Analytical approach to the metallomic of Nile tilapia (Oreochromis niloticus) liver tissue by SRXRF and FAAS after 2D-PAGE separation: preliminary results. Talanta, 82(3), 1052–1056. https://doi.org/10.1016/j.talanta.2010.06.023

    Article  CAS  PubMed  Google Scholar 

  22. Moraes PM, Santos FA, Padilha CCF, Vieira JCS, Zara LF, de Padilha PM (2012) A preliminary and qualitative metallomics study of mercury in the muscle of fish from Amazonas, Brazil. Biol Trace Elem Res 150(1–3):195–199. https://doi.org/10.1007/s12011-012-9502-x

    Article  CAS  PubMed  Google Scholar 

  23. Handbook, Shimadzu Cook (2007) "Atomic Absorption Spectrophotometry cookbook." Shimadzu Corporation. Kyoto. Japan

  24. Shevchenko A, Tomas H, Havli J, Olsen JV, Mann M (2007) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1(6):2856–2860. https://doi.org/10.1038/nprot.2006.468

    Article  CAS  Google Scholar 

  25. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. https://doi.org/10.1093/bioinformatics/bti610

    Article  CAS  PubMed  Google Scholar 

  26. Zar JH (2010) Bioestatistical analysis. Pretince Hall, New Jersey, p 944

    Google Scholar 

  27. da Silva EG, Jóia PR (2010) Questões Ambientais e Sócio Econômicas da Apicultura nos Municípios de Aquidauana e Anastácio-MS. Rev Pantaneira 12:37–43

    Google Scholar 

  28. Giannini TC, Acosta AL, Garófalo CA, Saraiva AM, Alves-dos-Santos I, Imperatriz-Fonseca VL (2012) Pollination services at risk: bee habitats will decrease owing to climate change in Brazil. Ecol Model 244:127–131

    Article  Google Scholar 

  29. Anderson L et al (1990) Metabolismo mineral. In: Nutrição. Guanabara Koogan, Rio de Janeiro, pp 63–92

    Google Scholar 

  30. Schmitzová J, Klaudiny J, Albert Š, Schröder W, Schreckengost W, Hanes J, Júdová J, Šimúth J (1998) A family of major royal jelly proteins of the honeybee Apis mellifera L. Cell Mol Life Sci CMLS 54(9):1020–1030. https://doi.org/10.1007/s000180050229

    Article  PubMed  Google Scholar 

  31. Yu F, Mao F, Jianke L (2010) Royal jelly proteome comparison between A. mellifera ligustica and A. cerana cerana. J Proteome Res 9(5):2207–2215. https://doi.org/10.1021/pr900979h

    Article  CAS  PubMed  Google Scholar 

  32. Hartfelder K, Makert GR, Judice CC, Pereira GAG, Santana WC, Dallacqua R, Bitondi MMG (2006) Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37(2):144–163. https://doi.org/10.1051/apido:2006013

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. UNESP - São Paulo State University, School of Veterinary Medicine and Animal Science, Botucatu, Brasil

    Wellington Luiz de Paula Araújo, Adriana Fava Negrão & Ricardo de Oliveira Orsi

  2. UNESP - São Paulo State University, Institute of Biosciences of Botucatu, Botucatu, Brasil

    José Cavalcante souza Vieira, Alis Correia Bittarello & Pedro de Magalhães Padilha

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  1. Wellington Luiz de Paula Araújo
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  2. Adriana Fava Negrão
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Correspondence to Wellington Luiz de Paula Araújo.

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de Paula Araújo, W.L., Negrão, A.F., Vieira, J.C.s. et al. Supplementation with an Inorganic Iron Source Modulates the Metalloproteomic Profile of the Royal Jelly Produced by Apis mellifera L.. Biol Trace Elem Res 195, 648–657 (2020). https://doi.org/10.1007/s12011-019-01863-8

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