Control of the microsporidian parasite Nosema ceranae in honey bees (Apis mellifera) using nutraceutical and immuno-stimulatory compounds
Autoři:
Daniel Borges aff001; Ernesto Guzman-Novoa aff001; Paul H. Goodwin aff001
Působiště autorů:
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada
aff001
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0227484
Souhrn
Nosema ceranae is a microsporidian parasite that causes nosemosis in the honey bee (Apis mellifera). As alternatives to the antibiotic fumagillin, ten nutraceuticals (oregano oil, thymol, carvacrol, trans-cinnmaldehyde, tetrahydrocurcumin, sulforaphane, naringenin, embelin, allyl sulfide, hydroxytyrosol) and two immuno-stimulatory compounds (chitosan, poly I:C) were examined for controlling N. ceranae infections. Caged bees were inoculated with N. ceranae spores, and treatments were administered in sugar syrup. Only two compounds did not significantly reduce N. ceranae spore counts compared to the infected positive control, but the most effective were sulforaphane from cruciferous vegetables, carvacrol from oregano oil, and naringenin from citrus fruit. When tested at several concentrations, the highest sulforaphane concentration reduced spore counts by 100%, but also caused 100% bee mortality. For carvacrol, the maximum reduction in spore counts was 57% with an intermediate concentration and the maximum bee mortality was 23% with the highest concentration. For naringenin, the maximum reduction in spore counts was 64% with the highest concentration, and the maximum bee mortality was only 15% with an intermediate concentration. In the longevity experiment, naringenin-fed bees lived as long as Nosema-free control bees, both of which lived significantly longer than infected positive control bees. While its antimicrobial properties may be promising, reducing sulforaphane toxicity to bees is necessary before it can be considered as a candidate for controlling N. ceranae. Although further work on formulation is needed with naringenin, its effect on extending longevity in infected bees may give it an additional value as a potential additive for bee feed in honey bee colonies.
Klíčová slova:
Death rates – Parasitic diseases – Antioxidants – Bees – Honey bees – Sulfides – Oils – Nosema
Zdroje
1. Keeling PJ, Fast NM. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology. 2002; 56:93–116. doi: 10.1146/annurev.micro.56.012302.160854 12142484
2. Goblirsch M. Nosema ceranae disease of the honey bee (Apis mellifera). Apidologie;49: 131–150.
3. Dussaubat C, Brunet JL, Higes M, Colbourne JK, Lopez J, Choi JH, et al. Gut pathology and responses to the Microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS One. 2012; 7: e37017. doi: 10.1371/journal.pone.0037017 22623972
4. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, et al. Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS One. 2013; 8: e72016. doi: 10.1371/journal.pone.0072016 23940803
5. Aufauvre J, Misme-Aucouturier B, Viguès B, Texier C, Delbac F, Blot N. Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS One. 2014; 9: e91686. doi: 10.1371/journal.pone.0091686 24646894
6. Martín-Hernández R, Meana A, Prieto L, Martínez-Salvador A, Garrido-Bailón E, Higes M. Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology. 2007; 73: 6331–6338. doi: 10.1128/AEM.00270-07 17675417
7. Chen Y, Evans JD, Smith IB, Pettis JS. 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. 2008; 97: 186–188. doi: 10.1016/j.jip.2007.07.010 17880997
8. Emsen B, Guzmán-Novoa E, Hamiduzzaman MM, Eccles L, Lacey B, Ruiz-Perez RA, et al. Higher prevalence and levels of Nosema ceranae than Nosema apis infections in Canadian honey bee colonies. Parasitology Research. 2016; 115: 175–181. doi: 10.1007/s00436-015-4733-3 26358102
9. Antúnez K, Martín-Hernández R, Prieto L, Meana A, Zunino P, Higes M. Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology. 2009; 11(9): 2284–2290. doi: 10.1111/j.1462-2920.2009.01953.x 19737304
10. Sinpoo C, Paxton RJ, Disayathanoowat T, Krongdang S, Chantawannakul P. Impact of Nosema ceranae and Nosema apis on individual worker bees of the two host species (Apis cerana and Apis mellifera) and regulation of host immune response. Journal of Insect Physiology. 2018; 105: 1–8. doi: 10.1016/j.jinsphys.2017.12.010 29289505
11. Martín-Hernández R, Botías C, Barrios L, Martínez-Salvador A, Meana A, Mayack C, et al. Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology Research. 2011; 109: 605–612. doi: 10.1007/s00436-011-2292-9 21360094
12. Higes M, Martín-Hernández R, Botías C, Bailón E, González-Porto AV, Barrios L, et al. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol. 2008; 10: 2659–2669. doi: 10.1111/j.1462-2920.2008.01687.x 18647336
13. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, et al. Colony collapse disorder: a descriptive study. PLoS One. 2009; 4:e6481. doi: 10.1371/journal.pone.0006481 19649264
14. Currie RW, Pernal SF, Guzman-Novoa E. Honey bee colony losses in Canada. Journal of Apicultural Research. 2010; 49:104–106.
15. Guzman-Novoa E. Colony collapse disorder and other threats to honey bees. In: One Health Case Studies: Addressing Complex Problems in a Changing World. Cork S., Hall D.C., & Liljebjelke K. (Eds). 5M Publishing Ltd, Sheffield, UK. 2016: 204–216.
16. Williams GR, Sampson MA, Shutler D, Rogers REL. Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? Journal of Invertebrate Pathology. 2008; 99: 342–344. doi: 10.1016/j.jip.2008.04.005 18550078
17. Higes M, Nozal MJ, Alvaro A, Barrios L, Meana A, Martín-Hernández R, et al. The stability and effectiveness of fumagillin in controlling Nosema ceranae (Microsporidia) infection in honey bees (Apis mellifera) under laboratory and field conditions. Apidologie. 2011; 42: 364–377.
18. Huang WF, Solter LF, Yau PM, Imai BS. Nosema ceranae escapes fumagillin control in honey bees. PLoS Pathogens. 2013; 9: e1003185. doi: 10.1371/journal.ppat.1003185 23505365
19. Brower V. Nutraceuticals: poised for a healthy slice of the healthcare market? Nature Biotechnology. 1998; 16: 728–731. doi: 10.1038/nbt0898-728 9702769
20. Devi AG, Sharma SD, Balavenkatasubbaiah M, Chandrasekharan K, Nayaka ARN, Kumar JJ. Identification of botanicals for the suppression of pebrine disease of the silkworm, Bombyx mori L. Uttar Pradesh Journal of Zoology. 2010; 30: 173–179.
21. Lee SH, Liu YT, Chen KM, Lii CK, Liu CT. Effect of garlic sulfur compounds on neutrophil infiltration and damage to the intestinal mucosa by endotoxin in rats. Food and Chemical Toxicology. 2012; 50: 567–574. doi: 10.1016/j.fct.2011.11.027 22138247
22. Kollanoor-Johny A, Upadhyay A, Baskaran SA, Upadhyaya I, Mooyottu S, Mishra N, et al. Effect of therapeutic supplementation of the plant compounds trans-cinnamaldehyde and eugenol on Salmonella enterica serovar Enteritidis colonization in market-age broiler chickens. Journal of Applied Poultry Research. 2012; 21:816–822.
23. Kim DK, Lillehoj HS, Lee SH, Jang SI, Bravo D. High-throughput gene expression analysis of intestinal intraepithelial lymphocytes after oral feeding of carvacrol, cinnamaldehyde, or Capsicum oleoresin. Poultry Science. 2010; 89:68–81. doi: 10.3382/ps.2009-00275 20008804
24. Yanaka A, Sato J, Ohmori S. Sulforaphane protects small intestinal mucosa from aspirin/NSAID-induced injury by enhancing host defense systems against oxidative stress and by inhibiting mucosal invasion of anaerobic Enterobacteria. Current Pharmaceutical Design. 2013; 19: 157–162. doi: 10.2174/13816128130120 22950492
25. Johansson NL, Pavia CS, Chiao JW. Growth inhibition of a spectrum of bacterial and fungal pathogens by sulforaphane, an isothiocyanate product found in broccoli and other cruciferous vegetables. Planta Medica. 2008; 74: 747–750. doi: 10.1055/s-2008-1074520 18484523
26. Assini JM, Mulvihill EE, Sutherland BG, Telford DE, Sawyez CG, Felder SL, et al. Naringenin prevents cholesterol-induced systemic inflammation, metabolic dysregulation, and atherosclerosis in Ldlr -/- mice. Journal of Lipid Research. 2013; 54: 711–724. doi: 10.1194/jlr.M032631 23269394
27. Amaro MI, Rocha J, Vila-Real H, Eduardo-Figueira M, Mota-Filipe H, Sepodes B, et al. Anti-inflammatory activity of naringenin and the biosynthesised naringenin by naringinase immobilized in microstructured materials in a model of DSS-induced colitis in mice. Food Research International. 2009; 42: 1010–1017.
28. Jayaraman J, Jesudoss VAS, Menon VP, Namasivayam N. Anti-inflammatory role of naringenin in rats with ethanol induced liver injury. Toxicology Mechanisms and Methods. 2012; 22: 568–576. doi: 10.3109/15376516.2012.707255 22900548
29. Schaffer S, Podstawa M, Visioli F, Bogani P, Müller WE, Eckert GP. Hydroxytyrosol-rich olive mill wastewater extract protects brain cells in vitro and ex vivo. Journal of Agricultural and Food Chemistry. 2007; 55: 5043–5049. doi: 10.1021/jf0703710 17530860
30. Rodríguez-Gutiérrez G, Duthie GG, Wood S, Morrice P, Nicol F, Reid M, et al. Alperujo extract, hydroxytyrosol, and 3,4-dihydroxyphenylglycol are bioavailable and have antioxidant properties in vitamin E-deficient rats—a proteomics and network analysis approach. Molecular Nutrition and Food Research. 2012; 56: 1131–1147.
31. Kumar GK, Dhamotharan R, Nagaraj MK, Srinivasa H, Murugesan S. Embelin ameliorates dextran sodium sulfate-induced colitis in mice. International Immunopharmacology. 2011; 11: 724–731. doi: 10.1016/j.intimp.2011.01.022 21296695
32. Chaudhari HS, Bhandari U, Khanna G. Preventive effect of embelin from Embelia ribes on lipid metabolism and oxidative stress in high-fat diet-induced obesity in rats. Planta Medica. 2012; 78: 651–657. doi: 10.1055/s-0031-1298379 22450777
33. Parvizi P, Mallick AI, Haq K, Schlegel B, Sharif S. A Toll-like receptor 3 agonist (poly I:C) elicits innate host responses in the spleen and lungs of chickens. The Canadian Journal of Veterinary Research. 2012; 76: 230–234. 23277704
34. Li C, Chen YX, Zhang S, Lü L, Chen YH, Chai J, et al. Identification, characterization, and function analysis of the Cactus gene from Litopenaeus vannamei. PLoS One. 2012; 7: e49711. doi: 10.1371/journal.pone.0049711 23185415
35. Huang RL, Deng ZY, Yang CB, Yin YL, Xie MY, Wu GY, et al. Dietary oligochitosan supplementation enhances immune status of broilers. Journal of the Science of Food and Agriculture. 2007; 87: 153–159.
36. Bogdan I, Mureşan E, Mureşan T, Mālaiu A, Nuelean V, Sabău A. Untersuchungen zur wirkung von ätherischen olen auf die Nosematose der bienen. Buletinul Institutului Agronomic Cluj-Napoca Seria Zootehnie si Medicina Veterinara. 1986; 40: 81–89.
37. Maistrello L, Lodesani M, Costa C, Leonardi F, Marani G, Caldon M, et al. Screening of natural compounds for the control of Nosema disease in honeybees (Apis mellifera). Apidologie. 2008; 39: 436–445.
38. Costa C, Lodesani M, Maistrello L. Effect of thymol and resveratrol administered with candy or syrup on the development of Nosema ceranae and on the longevity of honeybees (Apis mellifera L.) in laboratory conditions. Apidologie. 2010; 41: 141–150.
39. van den Heever JP, Thompson TS, Otto SJG, Curtis JM, Ibrahim A, Pernal SF. Evaluation of Fumagilin-B® and other potential alternative chemotherapies against Nosema ceranae-infected honeybees (Apis mellifera) in cage trial assays. Apidologie. 2016; 47: 617–630.
40. Strachecka AJ, Olszewski K, Paleolog J. Curcumin stimulates biochemical mechanisms of Apis mellifera resistance and extends the apian life-span. Journal of Apicultural Science. 2015; 59: 129–141.
41. Roussel M, Villay A, Delbac F, Michaud P, Laroche C, Roriz D, et al. Antimicrosporidian activity of sulphated polysaccharides from algae and their potential to control honeybee nosemosis. Carbohydrate Polymers. 2015; 133: 213–220. doi: 10.1016/j.carbpol.2015.07.022 26344274
42. Nanetti A, Rodriguez-García C, Meana A, Martín-Hernández R, Higes M. Effect of oxalic acid on Nosema ceranae infection. Research in Veterinary Science. 2015; 102: 167–172. doi: 10.1016/j.rvsc.2015.08.003 26412538
43. Ptaszyńska AA, Trytek M, Borsuk G, Buczek K, Rybicka-Jasińska K, Gryko D. Porphyrins inactivate Nosema spp. microsporidia. Scientific Reports. 2018; 8: 5523. doi: 10.1038/s41598-018-23678-8 29615690
44. Gary NE, Marston JM. Vacuum apparatus for collecting honey bees Hymenoptera-Apidae and other insects in trees. Annals of the Entomological Society of America. 1976; 69: 287–289.
45. Cantwell GE. Standard methods for counting Nosema spores. American Bee Journal. 1970; 110: 222–223.
46. Hamiduzzaman MM, Guzmán-Novoa E, Goodwin PH. A multiplex PCR assay to diagnose and quantify Nosema infections in honey bees (Apis mellifera). Journal of Invertebrate Pathology. 2010; 105: 151–155. doi: 10.1016/j.jip.2010.06.001 20570679
47. McGowan J, De la Mora A, Goodwin PH, Habash M, Hamiduzzaman MM, Kelly PG, et al. Viability and infectivity of fresh and cryopreserved Nosema ceranae spores. Journal of Microbiological Methods. 2016; 131: 16–22. doi: 10.1016/j.mimet.2016.09.021 27693753
48. Katznelson H., & Jamieson C.A. (1952). Control of Nosema disease of honeybees with fumagillin. Science; 115 (2977): 70–71. doi: 10.1126/science.115.2977.70 14913168
49. Tsinas A, Giannenas I, Voidarou C, Tzora A, Skoufos J. Effects of an oregano based dietary supplement on performance of broiler chickens experimentally infected with Eimeria acervulina and Eimeria maxima. Journal of Poultry Science. 2011; 48: 194–200.
50. Cho S, Choi Y, Park S, Park T. Carvacrol prevents diet-induced obesity by modulating gene expressions involved in adipogenesis and inflammation in mice fed with high-fat diet. Journal of Nutritional Biochemistry. 2012; 23: 192–201. doi: 10.1016/j.jnutbio.2010.11.016 21447440
51. Qin B, Dawson H, Polansky MM, Anderson RA. Cinnamon extract attenuates TNF-α-induced intestinal lipoprotein ApoB48 overproduction by regulating inflammatory, insulin, and lipoprotein pathways in enterocytes. Hormone and Metabolic Research. 2009; 41: 516–522. doi: 10.1055/s-0029-1202813 19593846
52. Nakmareong S, Kukongviriyapan U, Pakdeechote P, Donpunha W, Kukongviriyapan V, Kongyingyoes B, et al. Antioxidant and vascular protective effects of curcumin and tetrahydrocurcumin in rats with L-NAME-induced hypertension. Naunyn-Schmiedeberg’s Archives of Pharmacology. 2011; 383: 519–529. doi: 10.1007/s00210-011-0624-z 21448566
53. St Paul M, Brisbina JT, Abdul-Careemb MF, Sharif S. Immunostimulatory properties of Toll-like receptor ligands in chickens. Veterinary Immunology and Immunopathology. 2013; 152: 191–199. doi: 10.1016/j.vetimm.2012.10.013 23305711
54. Ebert TA, Kevan PG, Bishop BL, Kevan SD, Downer RA. Oral toxicity of essential oils and organic acids fed to honey bees (Apis mellifera). Journal of Apicultural Research and Bee World. 2007; 46: 220–224.
55. Gashout AH, Guzman-Novoa E. Acute toxicity of essential oils and other natural compounds to the parasitic mite Varroa destructor and to larval and adult worker honey bees (Apis mellifera L.). Journal of Apicultural Research. 2009; 48: 263–269.
56. Williams GR, Alaux C, Costa C, Csáki T, Doublet V, Eisenhardt D, et al. Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. Journal of Apicultural Research. 2013; 52(1): 1–35.
57. Wang YG, Zhang ZG, Guo WY, Sun WX, Miao X, Wu H, et al. Sulforaphane reduction of testicular apoptotic cell death in diabetic mice is associated with the upregulation of Nrf2 expression and function. American Journal of Physiology-Endocrinology and Metabolism. 2014; 307: E14–E23. doi: 10.1152/ajpendo.00702.2013 24801392
58. Holt HL, Aronstein KA, Grozinger CM. Chronic parasitization by Nosema microsporidia causes global expression changes in core nutritional, metabolic and behavioral pathways in honey bee workers (Apis mellifera). BMC Genomics. 2013; 14: 1–16.
59. Higes M, Juarranz A, Dias-Almeida J, Lucena S, Botías C, Meana A, et al. Apoptosis in the pathogenesis of Nosema ceranae (Microsporidia: Nosematidae) in honey bees (Apis mellifera). Environmental Microbiology Reports. 2013; 5: 530–536. doi: 10.1111/1758-2229.12059 23864567
60. Mentor S, Fisher D. Aggressive antioxidant reductive stress impairs brain endothelial cell angiogenesis and blood brain barrier function. Current Neurovascular Research. 2017; 14: 71–81. doi: 10.2174/1567202613666161129113950 27897111
61. Hu R, Khor TO, Shen G, Jeong WS, Hebbar V, Chen C, et al. Cancer chemoprevention of intestinal polyposis in ApcMin/+ mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis. 2006; 27: 2038–2046. doi: 10.1093/carcin/bgl049 16675473
62. Turgis M, Vu KD, Dupont C, Lacroix M. Combined antimicrobial effect of essential oils and bacteriocins against foodborne pathogens and food spoilage bacteria. Food Research International. 2012; 48: 696–702.
63. Bie JH, Wang J, Szomju B, Gehr TW, Ghosh S, Ghosh SS. Dietary supplement curcumin reduces inflammation and significantly improves glucose tolerance and atherosclerosis in LDLR -/- mice. Circulation. 2011; 124: a10870.
64. Kubota M, Shimizu M, Sakai H, Yasuda Y, Terakura D, Baba A, et al. Preventive effects of curcumin on the development of azoxymethane-induced colonic preneoplastic lesions in male C57BL/KsJ-db/db obese mice. Nutrition and Cancer. 2012; 64: 72–79. doi: 10.1080/01635581.2012.630554 22172229
65. Aronstein KA, Hayes GW. Antimicrobial activity of allicin against honey bee pathogens. Journal of Apicultural Research. 2004; 43: 57–59.
66. Porrini MP, Fernández NJ, Garrido PM, Gende LB, Medici SK, Eguaras MJ. In vivo evaluation of antiparasitic activity of plant extracts on Nosema ceranae (Microsporidia). Apidologie. 2011; 42: 700–707.
67. Saltykova ES, Karimova AA, Gataullin AR, Gaifullina LR, Matniyazov RT, Frolova MA, et al. The effect of high-molecular weight chitosans on the antioxidant and immune systems of the honeybee. Applied Biochemistry and Microbiology. 2016; 52: 553–557.
68. Li B, Su T, Chen X, Liu B, Zhu B, Fang Y, et al. Effect of chitosan solution on the bacterial septicemia disease of Bombyx mori (Lepidoptera: Bombycidae) caused by Serratia marcescens. Applied Entomology and Zoology. 2010; 45: 145–152.
69. Chattopadhyay D, Soumadeep S, Rishita C, Roy D, James J, Thirimurugan K. Context- and dose-dependent modulatory effects of naringenin on survival and development of Drosophila melanogaster. Biogerontology. 2016; 17(2): 383–39. doi: 10.1007/s10522-015-9624-6 26520643
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