Are commercial probiotics and prebiotics effective in the treatment and prevention of honeybee nosemosis C?

Parasitology Research

Volumn 115, Issue 1, 2016, Pages 397-406

  Ptaszyńska, Aneta A ^a   Borsuk, Grzegorz ^b   Zdybicka Barabas, Agnieszka ^a   Cytryńska, Małgorzata ^a   Małek, Wanda ^a  

^a MARIA CURIE SK ODOWSKA UNIVERSITY   (Poland)

^b UNIVERSITY OF LIFE SCIENCES IN LUBLIN   (Poland)

Author keywords

Apis mellifera survival; Lactobacillus rhamnosus, inulin; Nosema ceranae; Phenoloxidase activity; Prebiotic; Probiotic

Indexed keywords

INULIN; MONOPHENOL MONOOXYGENASE; PROBIOTIC AGENT; SUCROSE; SUGAR; FUNGAL DNA; PREBIOTIC AGENT;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; HEMOLYMPH; LACTOBACILLUS RHAMNOSUS; MALNUTRITION; MICROSPORIDIAN SPORE; MICROSPORIDIOSIS; MORTALITY; MORTALITY RATE; NONHUMAN; NOSEMOSIS; PRIORITY JOURNAL; SURVIVAL RATE; ANIMAL; APICULTURE; BEE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MULTIPLEX POLYMERASE CHAIN REACTION; NOSEMA; PATHOGENICITY; PHYSIOLOGY; PROCEDURES; RANDOMIZATION;

ANIMALS; BEEKEEPING; BEES; DNA, FUNGAL; HEMOLYMPH; INULIN; LACTOBACILLUS RHAMNOSUS; MONOPHENOL MONOOXYGENASE; MULTIPLEX POLYMERASE CHAIN REACTION; NOSEMA; PREBIOTICS; PROBIOTICS; RANDOM ALLOCATION;

EID: 84952984513     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-015-4761-z     Document Type: Article

References (72)

1. Ajitha SM, Sridhar M, Sridhar N, Singh ISB, Varghese V (2004) Probiotic effects of lactic acid bacteria against Vibrio alginolyticus in Penaeus (Fenneropenaeus) Indicus (H. Milne Edwards). Asian Fish Sci 17:71–80
2. Andrearczyk S, Kadhim MJ, Knaga S (2014) Influence of a probiotic on mortality, sugar syrup ingestion and infection of honeybees with Nosema spp. under laboratory assessment. Med Weter 70:762–765
3. Andrejko M, Zdybicka-Barabas A, Cytryńska M (2014) Diverse effects of Galleria mellonella infection with entomopathogenic and clinical strains of Pseudomonas aeruginosa. J Invertebr Pathol 115:14–25
4. Antúnez K, Martín-Hernández R, Prieto L, Meana A, Zunino P, Higes M (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ Microbiol 11:2284–2290
5. Audisio MC, Torres MJ, Sabaté DS, Ibarguren C, Apella MC (2011) Properties of different lactic acid bacteria isolated from Apis mellifera L. bee-gut. Microbiol Res. doi:10.1016/j.micres.2010.01.003
6. Audisio MC, Sabaté DC, Benítez-Ahrendts MR (2015) Effect of Lactobacillus johnsonii CRL1647 on different parameters of honeybee colonies and bacterial populations of the bee gut. Benefic Microbes 25:1–10. doi:10.3920/BM2014.0155
7. Bagheri T, Hedayati SA, Yavari V, Alizade M, Farzanfar A (2008) Growth, survival and gut microbial load of rainbow trout (Onchorhynchus mykiss) fry given diet supplemented with probiotic during the two months of first feeding. Turk J Fish Aquat Sci 8:43–48
8. Beney L, Gervais P (2001) Influence of the fluidity of the membrane on the response of microorganismsm to environmental stresses. Appl Microbiol Biotechnol 57:34–42
9. Borsuk G, Ptaszyńska AA, Olszewski K, Paleolog J (2013) Impact of nosemosis on the intestinal yeast flora of honey bee. Med Weter 69:76–730
10. Bradbear N (2009) Bees and their role in forest livelihood: a guide to the services provided by bees and the sustainable harvesting, processing and marketing of their products. Food and Agriculture Organization of the United Nations, Rome
11. Bradley TJ (2008) Active transport in insect recta. J Experim Biol 211:835–836
12. Cerenius L, Lee BL, Söderhäll K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263–271
13. Chaimanee V, Chantawannnakul P, Chen Y, Evans JD, Pettis JS (2012) Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J Insect Physiol 58:1090–1095
14. Conway PL (1989) Lactobacilli: fact and fiction. In: Grubb R (ed) The regulatory and protective role of the normal microflora. Macmillan Press, Basingstoke, pp 263–281
15. Corby-Harris V, Maes P, Anderson KE (2014) The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS ONE. doi:10.1371/journal.pone.0095056
16. Cummings JH, MacFarlane GT, Englyst HN (2001) Prebiotic digestion and fermentation. Am J Clin Nutr 73:415S–420S
17. Damiani N, Fernández NJ, Porrini MP, Podaza EA, Gende LB, Álvarez E, Buffa F, Brasesco C, Maggi MD, Marcangeli JA, Eguaras MJ (2014) Laurel leaf extracts for honeybee pest and disease management: antimicrobial, microsporicidal, and acaricidal activity. Parasitol Res 113:701–709
18. de Graaf DC, Masschelein G, Vandergeynst F, de Brabander HF, Jacobs FJ (1993) In vitro germination of Nosema apis (Microsporidia: Nosematidae) spores and its effect on their αα-trehalose/D-glucose ratio. J Invertebr Pathol 62:220–225
19. Douillard FP, Ribbera A, Kant R, Pietilä TE, Järvinen HM, Messing M et al (2013) Comparative genomic and functional analysis of 100 Lactobacillus rhamnosus strains and their comparison with strain GG. PLoS Genet. doi:10.1371/journal.pgen.1003683
20. Dussaubat C, Brunet J-L, Higes M, Colbourne JK, Lopez J, Choi J-H et al (2012) Gut pathology and responses to the Microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS ONE. doi:10.1371/journal.pone.0037017
21. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci 109:11002–11007
22. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H et al (2006) Immune pathways and defence mechanisms in honeybees Apis mellifera. Insect Mol Biol 15:645–656
23. Feigenbaum C, Naug D (2010) The influence of social hunger on food distribution and its implications for disease transmission in a honeybee colony. Insect Soc. doi:10.1007/s00040-010-0073-6
24. Forsgren E, Fries I (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol 170:212–217
25. Fries I, Chauzat M-P, Chen Y-P, Doublet V, Genersch E, Gisder S, et al. (2013) Standard methods for nosema research. In: Dietemann V, Ellis JD, Neumann P (eds) The COLOSS BEEBOOK: Volume II: Standard methods for Apis mellifera pest and pathogen research. J Apic Res. doi:10.3896/IBRA.1.52.1.14
26. Gliński Z, Buczek K (2003) Response of the Apoidea to fungal infections. Apiacta 38:183–189
27. Higes M, Garcia-Palencia P, Martín-Hernández R, Meana A (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol 94:211–217
28. Hornitzky M (2008) Nosema Disease – Literature review and three surveys of beekeepers – Part 2. Rural Industries Research and Development Corporation. Pub. No. 08/006
29. Hultmark D (2003) Drosophila immunity: paths and patterns. Curr Opin Immunol 15:12–19
30. Jack R, Tagg H, Ray B (1995) Bacteriocins of Gram-positive bacteria. Microbiol Rev 59:171–200
31. Malone LA, Gatehouse (née Edmonds) HS (1998) Effects of Nosema apis infection on honey bee (Apis mellifera) digestive proteolytic enzyme activity. J Invertebr Pathol 71:169–174
32. Martín-Hernández R, Meana A, Prieto L, Martínez Salvador A, Garrido-Bailón E, Higes M (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73:6331–6338
33. Martín-Hernández R, Botías C, Barrios L, Martínez-Salvador A, Meana A, Mayack C, Higes M (2011) Comparison of the energetic stress associated with experimental Nosema cerance and Nosema apis infection of honeybees (Apis mellifera). Parasitol Res 109:605–612
34. Martinson V, Danforth BN, Minckley R, Rueppell O, Tingek S, Moran N (2011) A simple and distinctive microbiota exclusively associated with honey bees and bumble bees. Mol Ecol. doi:10.1111/j.1365-294X.2010.04959.x/full
35. Mayack C, Naug D (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100:185–188
36. Mayack C, Naug D (2013) Individual energetic state can prevail over social regulation of foraging in honeybees. Behav Ecol Sociobiol 67:929–936
37. Naug D (2014) Infected honeybee foragers incur a higher loss in efficiency than in the rate of energetic gain. Biol Lett. doi:10.1098/rsbl.2014.0731
38. Naug D, Gibbs A (2009) Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 40:595–599
39. Nikoskelainen S, Salminen S, Bylund G, Ouwehand AC (2001) Characterization of the properties of human- and dairy-derived probiotics for prevention of infectious diseases in fish. Appl Environ Microbiol 67:2430–2435
40. Ötleş S (2013) Probiotics and prebiotics in food, nutrition and health. CRC Press, Boca Raton
41. Park SY, Kim CH, Jeong WH, Lee JH, Seo SJ, Han YS et al (2005) Effects of two hemolymph proteins on humoral defense reactions in the wax moth, Galleria mellonella. Dev Comp Immunol 29:43–51
42. Pătruică S, Hutu I (2013) Economic benefits of using prebiotic and probiotic products as supplements in stimulation feeds administered to bee colonies. Turk J Vet Anim Sci 37:259–263
43. Pătruică S, Mot D (2012) The effect of using prebiotic and probiotic products on intestinal micro-flora of the honeybee (Apis mellifera carpatica). Bull Entomol Res 102:619–623
44. Pattabhiramaiah M, Reddy MS, Brueckner D (2012) Detection of novel probiotic bacterium Lactobacillus spp. in the workers of Indian honeybee, Apis cerana indica. Int J Environ Sci. doi:10.6088/ijes.00202030002
45. Patterson JA, Burkholder KM (2003) Application of prebiotics and probiotics in poultry production. Poult Sci 82:627–631
46. Paxton RJ, Klee J, Korpela S, Fries I (2007) Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38:558–565
47. Porrini MP, Audisio MC, Sabate DC, Ibarguren C, Medici SK, Sarlo EG, Garrido PM, Eguaras MJ (2010) Effect of bacterial metabolites on microsporidian Nosema ceranae and on its host Apis mellifera. Parasitol Res 107:381–388. doi:10.1007/s00436-010-1875-1
48. Ptaszyńska AA, Borsuk G, Mułenko W, Olszewski K (2013) Impact of ethanol on Nosema spp. infected bees. Med Weter 69:736–741
49. Ptaszyńska AA, Borsuk G, Mułenko W, Demetraki-Paleolog J (2014) Differentiation of Nosema apis and Nosema ceranae spores under Scanning Electron Microscopy (SEM). J Apic Res. doi:10.3896/IBRA.1.53.5.02
50. Randazzo CL, Pitino I, Licciardello F, Muratore G, Caggia C (2013) Survival of Lactobacillus rhamnosus probiotic strains in peach jam during storage at different temperatures. Food Sci Technol (Campinas) 33:652–659
51. Roberfroid MB (2007) Prebiotics: the concept revisited. J Nutr 137:830S–837S
52. Roberts KE, Evison SEF, Baer B, Hughes WOH (2015) The cost of promiscuity: sexual transmission of Nosema microsporidian parasites in polyandrous honey bees. Sci Rep. doi:10.1038/srep10982
53. SAS Institute (2002–2003) SAS/STAT User’s Guide release 9.13, Cary, NC, Statistical Analysis System Institute
54. Schlundt J (2012) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a Joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. FAO/WHO
55. Schmid MR, Brockmann A, Perk CW, Stanley DW, Tautz J (2008) Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J Insect Physiol 54:439–444
56. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366
57. Slavin J (2013) Fiber and prebiotics: mechanisms and health benefits. Nutrients 5:1417–1435
58. Strachecka A, Olszewski K, Paleolog J, Borsuk G, Bajda M (2014) Coenzyme Q10 treatments influence the lifespan and key biochemical resistance systems in the honeybee, Apis mellifera. Arch Insect Biochem Physiol 86:165–179. doi:10.1002/arch.21159
59. Tajabadi N, Mardan M, Manap MYA, Shuhaim M, Meimandipour A, Nateghi L (2011) Detection and identification of Lactobacillus bacteria found in the honey stomach of the giant honeybee Apis dorasta. Apidologie 42:642–649
60. Tajabadi N, Mardan M, Manap MYA, Mustafa S (2013a) Molecular identification of Lactobacillus spp. isolated from the honey comb of the honey bee (Apis dorsata) by 16S rRNA gene sequencing. J Apic Res. doi:10.3896/IBRA.1.52.5.10
61. Tajabadi N, Mardan M, Saari N, Mustafa S, Bahreini R, Manap MYA (2013b) Identification of Lactobacillus plantarum, Lactobacillus pentosus and Lactobacillus fermentum from honey stomach of honeybee. Braz J Microbiol 44:717–722
62. Talpur AD, Memon AJ, Khan MI, Ikhwanuddin M, Danish D, Abol-Munafi AB (2012) Inhibition of pathogens by lactic acid bacteria and application as water additive multi isolates probiotics in early stages larviculture of P. pelagicus (Linnaeus, 1758). J Anim Plant Sci 22:54–64
63. Tymczyszyn EE, Gómez-Zavaglia A, Disalvo EA (2007) Effect of sugars and growth media on the dehydration of Lactobacillus delbrueckii ssp. bulgaricus. J Appl Microbiol 102:845–851. doi:10.1111/j.1365-2672.2006.03108.x
64. Urías-Silvas JE, Cani PD, Delmée E, Neyrinck A, López MG, Delzenne NM (2008) Physiological effects of dietary fructans extracted from Agave tequilana Gto. and Dasylirion spp. Br J Nutr 99:254–261. doi:10.1017/S0007114507795338
65. Vásquez A, Olofsson TC (2009) The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apic Res 48:189–195. doi:10.3896/IBRA.1.48.3.07
66. Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE. doi:10.1371/journal.pone.0033188.t002
67. Verlinden A, Hesta M, Millet S, Janssens GPJ (2006) Food allergy in dogs and cats: a review. Crit Rev Food Sci Nutr 46:259–273
68. Weese JS, Arroyo L (2003) Bacteriological evaluation of dog and cat diets that claim to contain probiotics. Can Vet J 44:212–215
69. Wilson AR, Sigee D, Epton HA (2005) Anti-bacterial activity of Lactobacillus plantarum strain SK1 against Listeria monocytogenes is due to lactic acid production. J Appl Microbiol 99:1516–1522
70. Wittner M, Weiss LM (1999) Microsporidia and microsporidiosis. ASM Press, Washington DC
71. Zdybicka-Barabas A, Cytryńska M (2010) Phenoloxidase activity in hemolymph of Galleria mellonella larvae challenged with Aspergillus oryzae. Ann UMCS Sect C (Biologia) 65:49–57
72. Zdybicka-Barabas A, Mak P, Jakubowicz T, Cytryńska M (2014) Lysozyme and defense peptides as suppressors of phenoloxidase activity in Galleria mellonella. Arch Insect Biochem Physiol 87:1–12