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Gram-Positive Bacteria with Probiotic Potential for the Apis mellifera L. Honey Bee: The Experience in the Northwest of Argentina

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Abstract

Apis mellifera L. is one of the most important natural pollinators of significant crops and flowers around the world. It can be affected by different types of illnesses: american foulbrood, nosemosis, varroasis, viruses, among others. Such infections mainly cause a reduction in honey production and in extreme situations, the death of the colony. Argentina is the world’s second largest honey exporter and the third largest honey producer, after China and Turkey. Given both the prominence of the honey bee in nature and the economic importance of apiculture in Argentina and the world, it is crucial to develop efficient and sustainable strategies to control honey bee diseases and to improve bee colony health. Gram-positive bacteria, such as lactic acid bacteria, mainly Lactobacillus, and Bacillus spp. are promising options. In the Northwest of Argentina, several Lactobacillus and Bacillus strains from the honey bee gut and honey were isolated by our research group and characterized by using in vitro tests. Two strains were selected because of their potential probiotic properties: Lactobacillus johnsonii CRL1647 and Bacillus subtilis subsp. subtilis Mori2. Under independent trials with both experimental and commercial hives, it was determined that each strain was able to elicit probiotic effects on bee colonies reared in the northwestern region of Argentina. One result was the increase in egg-laying by the queen which therefore produced an increase in bee number and, consequently, a higher honey yield. Moreover, the beneficial bacteria reduced the incidence of two important bee diseases: nosemosis and varroosis. These results are promising and extend the horizon of probiotic bacteria to the insect world, serving beekeepers worldwide as a natural tool that they can administer as is, or combine with other disease-controlling methods.

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References

  1. Klein AM, Vaissiere B, Cane J, Steffan-Dewenter I, Cunningham S, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol Sci 274:303–313

    Article  Google Scholar 

  2. Pott S, Biesmeijer J, Kremen C, Neumann P, Schweiger O, Kunin W (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  Google Scholar 

  3. Gilliam M, Taber S III (1991) Diseases, pests, and normal microflora of honeybees, Apis mellifera, from feral colonies. J Invert Pathol 58:286–289

    Article  Google Scholar 

  4. Gilliam M, Lorenz BJ (1983) Gram-positive cocci from apiarian sources. J Invert Pathol 42:187–195

    Article  Google Scholar 

  5. Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC (2015) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE 7:e33188

    Article  Google Scholar 

  6. Evans JD, Schwarz RS (2011) Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 19:614–620

    Article  CAS  Google Scholar 

  7. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci USA 109:11002–11007

    Article  CAS  Google Scholar 

  8. Audisio MC, Torres MJ, Sabaté DC, Ibarguren C, Apella MC (2011) Properties of different lactic acid bacteria isolated from Apis mellifera L. bee-gut. Microbiol Res 1:1–13

    Article  Google Scholar 

  9. Corby-Harris V, Maes P, Anderson KE (2015) The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS ONE 9:e95056

    Article  Google Scholar 

  10. Sabaté DC, Carrillo L, Audisio MC (2009) Inhibition of Paenibacillus larvae and Ascosphaera apis by Bacillus subtilis isolated from honeybee gut and honey samples. Res Microbiol 60:163–169

    Google Scholar 

  11. Gilliam M, Lorenz BJ, Richardson GV (1988) Digestive enzymes and micro-organisms in honey bees (Apis Melifera L.) influence of streptomycin, age, season and pollen. Microbios 55:95–114

    CAS  Google Scholar 

  12. Hamdi C, Balloi A, Essanaa J, Crotti E, Gonella E, Raddadi N, Ricci I, Boudabous A, Borin S, Manino A, Bandi C, Alma A, Daffonchio D, Cherif A (2011) Gut microbiote dysbiosis and honeybee health. J Appl Entomol 135:524–533

    Article  Google Scholar 

  13. Chambers MC, Schneider DS (2012) Pioneering immunology: insect style. Curr Opin Immunol 24:10–14

    Article  CAS  Google Scholar 

  14. Engel P, Kwong WK, McFrederick Q, Anderson KE, Barribeau SM, Chandler JA, Cornman RS, Dainat J, de Miranda JR, Doublet V, Emery O, Evans JD, Farinelli L, Flenniken ML, Granberg F, Grasis JA, Gauthier L, Hayer J, Koch H, Kocher S, Martinson VG, Moran N, Munoz-Torres M, Newton I, Paxton RJ, Powell E, Sadd BM, Schmid-Hempel P, Schmid-Hempel R, Song SJ, Schwarz RS, vanEngelsdorp D, Dainat B (2016) The bee microbiome: impact on bee health and model for evolution and ecology of host–microbe interactions. mBio 7:E02164-15. doi:10.1128/mBio.02164-15

  15. Alimentos argentinos (2014). http://www.alimentosargentinos.gob.ar/contenido/sectores/sectores.php?secc=otros

  16. Evans JD (2003) Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. J Invert Pathol 83:46–50

    Article  CAS  Google Scholar 

  17. Alippi AM, López AC, Reynaldy FJ, Grasso DH, Aguilar OM (2007) Evidence for plasmid-mediated tetracycline resistance in Paenibacillus larvae, the causal agent of American Foulbrood (AFB) disease in honeybees. Vet Microbiol 125:290–303

    Article  CAS  Google Scholar 

  18. Ollerton J, Winfree R, Tarrant S (2010) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Article  Google Scholar 

  19. Winston ML (1987) The biology of honey bee. Harvard University Press, Cambridge

    Google Scholar 

  20. Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin

    Book  Google Scholar 

  21. Wang Y, Ma LT, Xu BH (2015) Diversity in life history of queen and worker honey bees, Apis mellifera L. J Asia-Pacific Entomol 18:145–149

    Article  Google Scholar 

  22. Bashan A, Gibson TE, Friedman J, Carey VJ, Weiss ST, Hohmann EL, Liu YY (2016) Universality of human microbial dynamics. Nature 534:259–262

    Article  CAS  Google Scholar 

  23. Crotti E, Sansonno L, Prosdocimi EM, Vacchini V, Hamdi C, Cherif A, Gonella E, Marzorati M, Balloi A (2013) Microbial symbionts of honeybees: a promising tool to improve honeybee health. New Biotechnol 30:716–722

    Article  CAS  Google Scholar 

  24. Moran NA (2015) Genomics of the honey bee microbiome. Curr Opin Insect Sci 10:22–28

    Article  Google Scholar 

  25. Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384

    Article  CAS  Google Scholar 

  26. Kačániová M, Chlebo R, Kopernický M, Trakovická A (2004) Microflora of the honeybee gastrointestinal tract. Folia Microbiol 49:169–171

    Article  Google Scholar 

  27. Kačániová M, Pavlicová S, Hascík P, Kociubinski G, Kmazovická V, Sudzina M, Sudzinová J, Fikselová M (2009) Microbial communities in bees, pollen and honey from Slovakia. Acta Microbiol Immunol Hung 56:285–295

    Article  Google Scholar 

  28. McFrederick QS, Wcislo WT, Taylor DR, Ishak HD, Dowd SE, Mueller UG (2012) Environment or kin: whence do bees obtain acidophilic bacteria? Mol Ecol 21:1754–1768

    Article  Google Scholar 

  29. Tajabadi N, Mardan M, Saari N, Mustafa S, Bahreini R, Manap MYA (2016) Identification of Lactobacillus plantarum, Lactobacillus pentosus and Lactobacillus fermentum from honey stomach of honeybee. Brazilian J Microbiol 44:717–722

    Article  Google Scholar 

  30. Olofsson TC, Vásquez A (2008) Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Curr Microbiol 57:356–363

    Article  CAS  Google Scholar 

  31. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 20:285–295

    Article  Google Scholar 

  32. Moran NA, Hansen AK, Powell JE, Sabree ZL (2012) Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS ONE 7:1–10

    Google Scholar 

  33. Endo A, Salminen S (2013) Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Syst Appl Microbiol 36:444–448

    Article  Google Scholar 

  34. 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 7:e33188

    Article  Google Scholar 

  35. Snowdon JA, Cliver DO (1996) Microorganisms in honey. Int J Food Microbiol 31:1–26

    Article  CAS  Google Scholar 

  36. vanEngelsdorp D, Meixner MD (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invert Pathol 103:S80–S95

    Article  Google Scholar 

  37. Bogdanov S (2006) Contaminants of bee products. Apidologie 37:1–18

    Article  CAS  Google Scholar 

  38. Simon-Delso N, San Martin G, Bruneau E, Minsart LA, Mouret C, Hautier L (2014) Honeybee colony disorder in crop areas: the role of pesticides and viruses. PLoS ONE 9:e103073

    Article  Google Scholar 

  39. Kiljanek T, Niewiadowska A, Semeniuk S, Gaweł M, Borzęcka M, Posyniak A (2016) Multi-residue method for the determination of pesticides and pesticide metabolites in honeybees by liquid and gas chromatography coupled with tandem mass spectrometry-honeybee poisoning incidents. J Chromatogr A 1435:100

    Article  CAS  Google Scholar 

  40. Gregorc A, Ellis JD (2011) Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pest Biochem Physiol 99:200–207

    Article  CAS  Google Scholar 

  41. Genersch E (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invert Pathol 103:S10–S19

    Article  Google Scholar 

  42. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119

    Article  Google Scholar 

  43. Higes M, Meana A, Bartolomé C, Botías C, Martín-Hernández R (2013) Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol 5:17–29

    Article  Google Scholar 

  44. Maggi MD, Antúnez K, Invernizzi C, Aldea P, Vargas M, Negri P, Brasesco C, De Jong D, Message D, Teixeira EW, Principal J, Barrios C, Ruffinengo S, Rodríguez Da Silva R, Eguaras MJ (2016) Honeybee health in South America. Apidologie. doi:10.1007/s13592-016-0445-7

    Google Scholar 

  45. Traver BE, Fell RD (2011) Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia. J Invert Pathol 107:43–49

    Article  Google Scholar 

  46. Rogers REL, Williams GR (2007) Honey bee health in crisis: what is causing bee mortality? Am Bee J 147:441

    Google Scholar 

  47. Ratnieks FLW, Carreck NL (2010) Clarity on honey bee collapse? Science 327:152–153

    Article  CAS  Google Scholar 

  48. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, Frazier M, Frazier J, Cox-Foster D, Chen Y, Underwood R, Tarpy DR, Pettis JS (2009) Colony collapse disorder: a descriptive study. PLoS ONE 4:e6481

    Article  Google Scholar 

  49. Gilliam M, Morton HL (1978) Bacteria belonging to the genus Bacillus isolated from honey bees, Apis mellifera, fed 2,4-d and antibiotics. Apidologie 9:213–222

    Article  Google Scholar 

  50. Miyagi T, Peng CYS, Chuang RY, Mussen EC, Spivak MS, Doi RH (2000) Verification of oxytetracycline-resistant American foulbrood pathogen Paenibacillus larvae in the United States. J Invert Pathol 75:95–96

    Article  CAS  Google Scholar 

  51. Barnett EA, Charlton AJ, Fletcher MR (2007) Incidents of bee poisoning with pesticides in the United Kingdom, 1994–2003. Pest Manag Sci 63:1051–1057

    Article  CAS  Google Scholar 

  52. Martel AC, Zeggane S, Drajnudel P, Faucon JP, Aubert M (2006) Tetracycline residues in honey after hive treatment. Food Addit Contam 23:265–273

    Article  CAS  Google Scholar 

  53. Sheridan R, Policastro B, Thomas S, Rice D (2008) Analysis and occurrence of 14 sulfonamide antibacterials and chloramphenicol in honey by solid-phase extraction followed. J Agric Food Chem 56:3509–3516

    Article  CAS  Google Scholar 

  54. Fuller R (1991) Probiotics in human medicine. Gut 32:439–442

    Article  CAS  Google Scholar 

  55. Reid G (2016) Probiotics: definition, scope and mechanisms of action. Best Pract Res Clin Gastroenterol 30:17–25

    Article  CAS  Google Scholar 

  56. Sanders ME (2016) Probiotics and microbiota composition. BMC Med 14:82

    Article  Google Scholar 

  57. Lee YK, Salminen S (2009) Handbook of probiotics and prebiotics, 2nd edn. Wiley, New Jersey, pp 14–19

    Google Scholar 

  58. Fuchs-Tarlovsky V, Marquez-Barba MF, Sriram K (2016) Probiotics in dermatologic practice. Nutrition 32:289–295

    Article  Google Scholar 

  59. Muñoz-Atienza E, Araújo C, Magadán S, Hernández PE, Herranz C, Santos Y, Cintas LM (2014) In vitro and in vivo evaluation of lactic acid bacteria of aquatic origin as probiotics for turbot (Scophthalmus maximus L.) farming. Fish Shellfish Immunol 41:570–580

    Article  Google Scholar 

  60. Katz E, Demain AL (1977) The peptide antibiotics of Bacillus: chemistry, biogenesis, and possible functions. Bacteriol Rev 41:449–474

    CAS  Google Scholar 

  61. Loiseau C, Schlusselhuber M, Bigot R, Bertaux J, Berjeaud JM, Verdon J (2015) Surfactin from Bacillus subtilis displays an unexpected anti-Legionella activity. Appl Microbiol Biotechnol 99:5083–5093

    Article  CAS  Google Scholar 

  62. Cochrane SA, Vederas JC (2016) Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med Res Rev 36:4–31

    Article  CAS  Google Scholar 

  63. Sabaté DC, Audisio MC (2013) Inhibitory activity of surfactin, produced by different Bacillus subtilis subsp. subtilis strains, against Listeria monocytogenes sensitive and bacteriocin-resistant strains. Microbiol Res 168:125–129

    Article  Google Scholar 

  64. Torres MJ, Petroselli G, Daz M, Erra-Balsells R, Audisio MC (2015) Bacillus subtilis subsp. subtilis CBMDC3f with antimicrobial activity against Gram-positive foodborne pathogenic bacteria. UV-MALDI-TOF MS analysis of its bioactive compounds. World J Microbiol Biotechnol 31:929–940

    Article  CAS  Google Scholar 

  65. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125

    Article  CAS  Google Scholar 

  66. Hong HA, Duc LH, Cutting SM (2005) The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 29:813–835

    Article  CAS  Google Scholar 

  67. Cutting SM (2011) Bacillus probiotics. Food Microbiol 28:214–220

    Article  Google Scholar 

  68. Williams P (2007) Bacillus subtilis: a shocking message from a probiotic. Cell Host Microbe 1:248–249

    Article  CAS  Google Scholar 

  69. Urdaci MC, Jacquot C, Racedo SM, Rambert J, Pinchuk IV (2016) Tu2027 Probiotic Bacillus subtilis attenuate inflammation in a rat model of arthritis through modulation of intestinal microbiota. Gastroenterol 150:S1009

    Article  Google Scholar 

  70. Li Y, Xu Q, Huang Z, Lv L, Liu X, Yin C, Yan H, Yuan J (2016) Effect of Bacillus subtilis CGMCC 1.1086 on the growth performance and intestinal microbiota of broilers. J Appl Microbiol 120:195–204

    Article  CAS  Google Scholar 

  71. Lazado CC, Marlowe C, Caipang A (2014) Mucosal immunity and probiotics in fish. Fish Shellfish Immunol 39:78–89

    Article  CAS  Google Scholar 

  72. Hai NV (2015) Research findings from the use of probiotics in tilapia aquaculture: a review. Fish Shellfish Immunol 45:592–597

    Article  CAS  Google Scholar 

  73. Fritze D (2004) Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathol 94:1245–1248

    Article  Google Scholar 

  74. Logan NA, De Vos P (2009) Genus I Bacillus. In: Goodfellow M, Kämpfer P (eds) Bergey’s manual of systematic bacteriology. Vol III. The Firmicutes, 2nd edn. Springer, Athens, pp 21–36

    Google Scholar 

  75. Mohr KI, Tebbe CC (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Env Microbiol 8:258–272

    Article  CAS  Google Scholar 

  76. Olofsson TC, Alsterfjord M, Nilson B, Butler E, Vásquez A (2014) Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov. and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. Int J Syst Evol Microbiol 64:3109–3119

    Article  Google Scholar 

  77. Oelschlaeger TA (2010) Mechanisms of probiotic actions—a review. Int J Med Microbiol 399:57–62

    Article  Google Scholar 

  78. O’Shea EF, Cotter PD, Stanton C, Ross RP, Hill C (2012) Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int J Food Microbiol 152:189–205

    Article  Google Scholar 

  79. Kanmani P, Satish Kumar R, Yuvaraj N, Paari KA, Pattukumar V, Arul V (2013) Probiotics and its functionally valuable products—a review. Crit Rev Food Sci Nutr 53:641–658

    Article  CAS  Google Scholar 

  80. Máchová M, Rada V, Huk J, Smékal F (1997) Development of probiotics for bees. Apiacta 4:99–111

    Google Scholar 

  81. Evans JD, Lopez DL (2004) Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). J Econ Entomol 97:752–756

    Article  CAS  Google Scholar 

  82. Pătruică S, Mot D (2012) The effect of using prebiotic and probiotic products on intestinal microflora of the honeybee (Apis mellifera carpatica). Bull Entomol Res 102:619–623

    Article  Google Scholar 

  83. Pătruică S, Dumitrescu G, Stancu A, Bura M, Bănăţean Dunea I (2012) The effect of prebiotic and probiotic feed supplementation on the wax glands of worker bees (Apis mellifera). J Anim Sci Biotechnol 45:268–271

    Google Scholar 

  84. Andrearczyk S, Kadhim MJ, Knaga S (2014) Influence of a probiotic on the mortality, sugar syrup ingestion and infection of honeybees with Nosema spp. under laboratory assessment. Med Water 70:762–765

    Google Scholar 

  85. Ptaszyńska AA, Borsuk G, Zdybicka-Barabas A, Małgorzata Cytryńska M, Małek W (2016) Are commercial probiotics and prebiotics effective in the treatment and prevention of honeybee nosemosis C? Parasitol Res 115:397–406

    Article  Google Scholar 

  86. Salminen S, Deighton MA, Benno Y, Gorbach SL (1998) Lactic acid bacteria in health and disease. In: Salminen S, von Wright A (eds) Lactic acid bacteria. Microbiology and functional aspects, 2nd edn. Marcel Dekker, New York, pp 211–253

    Google Scholar 

  87. Saarela M, Mogensen G, Fondén R, Mättö J, Mattila-Sandholm T (2000) Probiotic bacteria: safety, functional and technological properties. J Biotechnol 84:197–215

    Article  CAS  Google Scholar 

  88. Grześkowiak L, Endo A, Beasley S, Salminen S (2015) Microbiota and probiotics in canine and feline welfare. Anaerobe 34:14–23

    Article  Google Scholar 

  89. Audisio MC, Benítez-Ahrendts MR (2011) Lactobacillus johnsonii CRL1647, isolated from Apis mellifera L. bee-gut, exhibited a beneficial effect on honeybee colonies. Benef Microbes 2:29–34

    Article  CAS  Google Scholar 

  90. Audisio MC, Sabaté DC, Benítez-Ahrendts MR (2015) Effect of Lactobacillus johnsonii CRL1647 on different parameters of honeybee colonies and on defined culturable bacterial populations of bee gut. Benef Microbes 25:1–10

    Google Scholar 

  91. Gilliam M, Valentine DK (1976) Bacteria isolated from intestinal contents of foraging worker honey bees, Apis mellifera: the genus Bacillus. J Invert Pathol 28:275–276

    Article  Google Scholar 

  92. Sabaté DC, Cruz MS, Benítez-Ahrendts MR, Audisio MC (2012) Beneficial effects of Bacillus subtilis subsp. subtilis Mori2, a honey associated strain, on honeybee colony performance. Probiotics Antimicrob Proteins 4:39–46

    Article  Google Scholar 

  93. Jack R, Tagg H, Ray B (1995) Bacteriocins of Gram-positive bacteria. Microbiol Rev 59:171–200

    CAS  Google Scholar 

  94. Ibarguren C, Raya RR, Apella MC, Audisio MC (2010) Enterococcus faecium isolated from honey synthesized bacteriocin-like substances active against different Listeria monocytogenes strains. J Microbiol 48:44–52

    Article  CAS  Google Scholar 

  95. Soria MC, Audisio MC (2014) Inhibition of Bacillus cereus strains by antimicrobial metabolites from Lactobacillus johnsonii CRL1647 and Enterococcus faecium SM21. Probiotics Antimicrob Proteins 6:208–216

    Article  CAS  Google Scholar 

  96. Torres MJ, Pérez Brandan C, Petroselli G, Erra-Balsells R, Audisio MC (2016) Antagonistic effects of Bacillus subtilis subsp. subtilis and B. amyloliquefaciens against Macrophomina phaseolina: SEM study of fungal changes and UV-MALDI-TOF MS analysis of their bioactive compounds. Microbiol Res 182:31–39

    Article  CAS  Google Scholar 

  97. Yoshiyama M, Wu M, Sugimura Y, Takaya N, Kimoto-Nira H, Suzuki C (2013) Inhibition of Paenibacillus larvae by lactic acid bacteria isolated from fermented materials. J Invert Pathol 112:62–67

    Article  CAS  Google Scholar 

  98. Porrini MP, Audisio MC, Sabaté 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

    Article  Google Scholar 

  99. Maggi MD, Negri P, Plischuk S, Szawarski N, De Piano F, De Feudis L, Eguaras MJ, Audisio MC (2013) Effects of the organic acids produced by a lactic acid bacterium in Apis mellifera colony development, Nosema ceranae control and fumagillin efficiency. Vet Microbiol 167:474–483

    Article  CAS  Google Scholar 

  100. Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309

    Article  CAS  Google Scholar 

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Acknowledgments

The work at the Laboratory of Applied Bacteriology of INIQUI-CONICET, UNSa has been supported by grants from CONICET, CIUNSa and ANPCyT. Dr. Audisio is a Research Member of CONICET, Argentina.

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Audisio, M.C. Gram-Positive Bacteria with Probiotic Potential for the Apis mellifera L. Honey Bee: The Experience in the Northwest of Argentina. Probiotics & Antimicro. Prot. 9, 22–31 (2017). https://doi.org/10.1007/s12602-016-9231-0

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