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The promise of probiotics in honeybee health and disease management

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Abstract

Over the last decades, losses of bee populations have been observed worldwide. A panoply of biotic and abiotic factors, as well as the interplay among them, has been suggested to be responsible for bee declines, but definitive causes have not yet been identified. Among pollinators, the honeybee Apis mellifera is threatened by various diseases and environmental stresses, which have been shown to impact the insect gut microbiota that is known to be fundamental for host metabolism, development and immunity. Aimed at preserving the gut homeostasis, many researches are currently focusing on improving the honeybee health through the administration of probiotics e.g., by boosting the innate immune response against microbial infections. Here, we review the knowledge available on the characterization of the microbial diversity associated to honeybees and the use of probiotic symbionts as a promising approach to maintain honeybee fitness, sustaining a healthy gut microbiota and enhancing its crucial relationship with the host immune system.

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Data availability

The data that support the findings of this study are available from the corresponding author upon request.

References

  • Abdi K et al (2018) Parasites-Iflavirus association and emergence of three master variants of DWV affecting Apis mellifera intermissa in Tunisian apiaries. Bull Insectol 71:273–282

    Google Scholar 

  • Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918

    Article  CAS  PubMed  Google Scholar 

  • Alippi AM (2000) Is Terramycin® losing its effectiveness against AFB. Bee Biz 11:27–29

    Google Scholar 

  • Aljedani DM (2022) Antibiotic treatment (Tetracycline) effect on bio-efficiency of the larvae honey bee (Apis mellifera jemenatica). Saudi J Biol Sci 29:1477–1486

    Article  CAS  PubMed  Google Scholar 

  • Anderson KE, Ricigliano VA (2017) Honey bee gut dysbiosis: a novel context of disease ecology. Curr Opin Insect Sci 22:125–132

    Article  PubMed  Google Scholar 

  • Audisio MC (2017) Gram-positive bacteria with probiotic potential for the Apis mellifera L. honey bee: the experience in the northwest of Argentina. Probiotics Antimicrob Proteins 9:22–31

    Article  CAS  PubMed  Google Scholar 

  • 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 166:1–13

    Article  Google Scholar 

  • Audisio MC, Sabate DC, Benítez-Ahrendts MR (2015) Effect of Lactobacillus johnsonii CRL1647 on different parameters of honeybee colonies and bacterial populations of the bee gut. Beneficial Microbes 6:687–695

    Article  CAS  PubMed  Google Scholar 

  • Babendreier D, Joller D, Romeis J, Bigler F, Widmer F (2006) Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol 59:600–610

    Article  Google Scholar 

  • Bailey L (1983) Melissococcus pluton, the cause of European foulbrood of honey bees (Apis spp.). J Appl Bacteriol 55:65–69

    Article  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Barrasso R, Bonerba E, Savarino AE, Ceci E, Bozzo G, Tantillo G (2018) Simultaneous quantitative detection of six families of antibiotics in honey using a biochip multi-array technology. Veterinary Sciences 6:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Baud D, Dimopoulou Agri V, Gibson GR, Reid G, Giannoni E (2020) Using probiotics to flatten the curve of coronavirus disease COVID-2019 pandemic. Front Public Health 8:186

    Article  PubMed  PubMed Central  Google Scholar 

  • BenVau LR, Nieh JC (2017) Larval honey bees infected with Nosema ceranae have increased vitellogenin titers as young adults. Sci Rep 7:14144

    Article  PubMed  PubMed Central  Google Scholar 

  • Bleau N, Bouslama S, Giovenazzo P, Derome N (2020) Dynamics of the honeybee (Apis mellifera) gut microbiota throughout the overwintering period in Canada. Microorganisms 8:1146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonilla-Rosso G, Engel P (2018) Functional roles and metabolic niches in the honey bee gut microbiota. Curr Opin Microbiol 43:69–76

    Article  CAS  PubMed  Google Scholar 

  • Bonilla-Rosso G et al (2019) Acetobacteraceae in the honey bee gut comprise two distant clades with diverging metabolism and ecological niches. bioRxiv 861260:41–50

  • Bottacini F et al (2012) Bifidobacterium asteroides PRL2011 genome analysis reveals clues for colonization of the insect gut. PLoS ONE 7:e44229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozkurt HS, Quigley EM (2020) The probiotic Bifidobacterium in the management of Coronavirus: a theoretical basis. Int J Immunopathol Pharmacol 34:2058738420961304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bromenshenk JJ et al (2010) Iridovirus and microsporidian linked to honey bee colony decline. PLoS ONE 5:e13181

    Article  PubMed  PubMed Central  Google Scholar 

  • Buchon N, Broderick NA, Lemaitre B (2013) Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat Rev Microbiol 11:615–626

    Article  CAS  PubMed  Google Scholar 

  • Bulson L, Becher MA, McKinley TJ, Wilfert L (2021) Long-term effects of antibiotic treatments on honeybee colony fitness: a modelling approach. J Appl Ecol 58:70–79

    Article  CAS  PubMed  Google Scholar 

  • Callegari M et al (2021) Compartmentalization of bacterial and fungal microbiomes in the gut of adult honeybees. Npj Biofilms Microbiomes 7:1–15

    Article  Google Scholar 

  • Castelli L, Branchiccela B, Romero H, Zunino P, Antúnez K (2022) Seasonal dynamics of the honey bee gut microbiota in colonies under subtropical climate. Microb Ecol 83:492–500

    Article  CAS  PubMed  Google Scholar 

  • Colombel J (1987) Yogurt with Bifidobacterium longum reduces erythromycin-induced gastrointestinal effects. Lancet 2:8549

    Google Scholar 

  • Corby-Harris V, Maes P, Anderson KE (2014a) The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS ONE 9:e95056

    Article  PubMed  PubMed Central  Google Scholar 

  • Corby-Harris V, Snyder LA, Schwan MR, Maes P, McFrederick QS, Anderson KE (2014b) Origin and effect of alpha 2.2 Acetobacteraceae in honey bee larvae and description of Parasaccharibacter apium gen. nov., sp. nov. Appl Environ Microbiol 80:7460–7472

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornman RS et al (2012) Pathogen webs in collapsing honey bee colonies. PLoS ONE 7:e43562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox-Foster DL et al (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283–287

    Article  CAS  PubMed  Google Scholar 

  • Crotti E et al (2010) Acetic acid bacteria, newly emerging symbionts of insects. Appl Environ Microbiol 76:6963–6970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crotti E et al (2013) Microbial symbionts of honeybees: a promising tool to improve honeybee health. New Biotechnol 30:716–722

    Article  CAS  Google Scholar 

  • Daisley BA et al (2020a) Novel probiotic approach to counter Paenibacillus larvae infection in honey bees. ISME J 14:476–491

    Article  CAS  PubMed  Google Scholar 

  • Daisley BA et al (2020b) Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees. Commun Biol 3:1–13

    Article  Google Scholar 

  • Daisley BA, Pitek AP, Mallory E, Chernyshova AM, Allen-Vercoe E, Reid G, Thompson GJ (2022) Disentangling the microbial ecological factors impacting honey bee susceptibility to Paenibacillus larvae infection. Trends Microbiol. https://doi.org/10.1016/j.tim.2022.11.012

    Article  PubMed  Google Scholar 

  • de Jong W et al (2019) Effects of diets containing different concentrations of pollen and pollen substitutes on physiology, Nosema burden, and virus titers in the honey bee (Apis mellifera L.). Apidologie 50:845–858

    Article  Google Scholar 

  • Dobbelaere W, de Graaf DC, Peeters JE (2001) Development of a fast and reliable diagnostic method for American foulbrood disease (Paenibacillus larvae subsp. larvae) using a 16S rRNA gene based PCR. Apidologie 32:363–370

    Article  CAS  Google Scholar 

  • Dong Z-X et al (2020) Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiol Res 231:126370

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engel P, Kwong WK, Moran NA (2013) Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera. Int J Syst Evol Microbiol 63:3646–3651

    Article  CAS  PubMed  Google Scholar 

  • Engel P, Stepanauskas R, Moran NA (2014) Hidden diversity in honey bee gut symbionts detected by single-cell genomics. PLoS Genet 10:e1004596

    Article  PubMed  PubMed Central  Google Scholar 

  • Engel P, Bartlett KD, Moran NA (2015) The bacterium Frischella perrara causes scab formation in the gut of its honeybee host. Mbio 6:e00193-e1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erkosar B, Leulier F (2014) Transient adult microbiota, gut homeostasis and longevity: novel insights from the Drosophila model. FEBS Lett 588:4250–4257

    Article  CAS  PubMed  Google Scholar 

  • Evans JD (2004) Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. J Invertebr Pathol 85:105–111

    Article  CAS  PubMed  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Evans J et al (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15:645–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fries I (2010) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103:S73–S79

    Article  PubMed  Google Scholar 

  • Fries I et al (2013) Standard methods for Nosema research. J Apic Res 52:1–28

    Article  Google Scholar 

  • Fuller R (1992) History and development of probiotics. probiotics. Springer, Dordrecht, pp 1–8

    Chapter  Google Scholar 

  • Genersch E (2008) Paenibacillus larvae and American foulbrood–long since known and still surprising. J Verbr Lebensm 3:429–434

    Article  Google Scholar 

  • Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97

    Article  CAS  PubMed  Google Scholar 

  • Gochnauer T (1951) Drugs fight foulbrood disease in bees. Minn Home Fam Sci 9:15

    Google Scholar 

  • Gorbach S, Chang T-W, Goldin B (1987) Successful treatment of relapsing Clostridium difficile colitis with Lactobacillus GG. The Lancet 330:1519

    Article  Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208

    Article  CAS  PubMed  Google Scholar 

  • Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957

    Article  PubMed  Google Scholar 

  • Gourbeyre P, Denery S, Bodinier M (2011) Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J Leukoc Biol 89:685–695

    Article  CAS  PubMed  Google Scholar 

  • Grau T, Vilcinskas A, Joop G (2017) Sustainable farming of the mealworm Tenebrio molitor for the production of food and feed. Zeitschrift Für Naturforschung C 72:337–349

    Article  CAS  Google Scholar 

  • Greenleaf SS, Kremen C (2006) Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc Natl Acad Sci 103:13890–13895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamdi C et al (2011) Gut microbiome dysbiosis and honeybee health. J Appl Entomol 135:524–533

    Article  Google Scholar 

  • Härtel C et al (2017) Lactobacillus acidophilus/Bifidobacterium infantis probiotics are associated with increased growth of VLBWI among those exposed to antibiotics. Sci Rep 7:5633

    Article  PubMed  PubMed Central  Google Scholar 

  • Hatjina F et al (2011) Polar tube protein gene diversity among Nosema ceranae strains derived from a Greek honey bee health study. J Invertebr Pathol 108:131–134

    Article  CAS  PubMed  Google Scholar 

  • Higes M, Martín R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92:93–95

    Article  CAS  PubMed  Google Scholar 

  • Higes M, García-Palencia P, Martín-Hernández R, Meana A (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol 94:211–217

    Article  PubMed  Google Scholar 

  • Higes M et al (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10:2659–2669

    Article  PubMed  Google Scholar 

  • Hill C et al (2014) The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514

    Article  PubMed  Google Scholar 

  • Hroncova Z, Killer J, Hakl J, Titera D, Havlik J (2019) In-hive variation of the gut microbial composition of honey bee larvae and pupae from the same oviposition time. BMC Microbiol 19:1–8

    Article  Google Scholar 

  • Huang Z (2012) Pollen nutrition affects honey bee stress resistance. Terr Arthropod Rev 5:175–189

    Article  Google Scholar 

  • Huang Q, Kryger P, Le Conte Y, Moritz RF (2012) Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. J Invertebr Pathol 109:297–302

    Article  PubMed  Google Scholar 

  • Huang W-F, Solter LF, Yau PM, Imai BS (2013) Nosema ceranae escapes fumagillin control in honey bees. PLoS Pathog 9:e1003185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iorizzo M et al (2022) Functional properties and antimicrobial activity from lactic acid bacteria as resources to improve the health and welfare of honey bees. InSects 13:308

    Article  PubMed  PubMed Central  Google Scholar 

  • Jia H-R et al (2016) The effects of Bt Cry1Ie toxin on bacterial diversity in the midgut of Apis mellifera ligustica (Hymenoptera: Apidae). Sci Rep 6:24664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston BC, Goldenberg JZ, Parkin PC (2016) Probiotics and the prevention of antibiotic-associated diarrhea in infants and children. JAMA 316:1484–1485

    Article  PubMed  Google Scholar 

  • Kačániová M, Gasper J, Terentjeva M (2021) Antagonistic effect of gut microbiota of honeybee (Apis mellifera) against causative agent of American foulbrood Paenibacillus larvae. J Microbiol Biotechnol Food Sci 2021:478–481

    Google Scholar 

  • Kakumanu ML, Reeves AM, Anderson TD, Rodrigues RR, Williams MA (2016) Honey bee gut microbiome is altered by in-hive pesticide exposures. Front Microbiol 7:1255

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kapheim KM, Rao VD, Yeoman CJ, Wilson BA, White BA, Goldenfeld N, Robinson GE (2015) Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS ONE 10:e0123911

    Article  PubMed  PubMed Central  Google Scholar 

  • Kešnerová L, Moritz R, Engel P (2016) Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. Int J Syst Evol Microbiol 66:414–421

    Article  PubMed  Google Scholar 

  • Kešnerová L, Emery O, Troilo M, Liberti J, Erkosar B, Engel P (2020) Gut microbiota structure differs between honeybees in winter and summer. ISME J 14:801–814

    Article  PubMed  Google Scholar 

  • Klein A-M et al (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond b Biol Sci 274:303–313

    Google Scholar 

  • Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci 108:19288–19292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kochansky J, Knox DA, Feldlaufer M, Pettis JS (2001) Screening alternative antibiotics against oxytetracycline-susceptible and-resistant Paenibacillus larvae. Apidologie 32:215–222

    Article  CAS  Google Scholar 

  • Kowallik V, Mikheyev AS (2021) Honey bee larval and adult microbiome life stages are effectively decoupled with vertical transmission overcoming early life perturbations. Mbio 12:e02966-e3021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kujawa-Szewieczek A, Adamczak M, Kwiecień K, Dudzicz S, Gazda M, Więcek A (2015) The effect of Lactobacillus plantarum 299v on the incidence of Clostridium difficile infection in high risk patients treated with antibiotics. Nutrients 7:10179–10188

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwong WK, Moran NA (2013) Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. Int J Syst Evol Microbiol 63:2008–2018

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwong WK, Mancenido AL, Moran NA (2017) Immune system stimulation by the native gut microbiota of honey bees. R Soc Open Sci 4:170003

    Article  PubMed  PubMed Central  Google Scholar 

  • Larsson DG, Flach CF (2022) Antibiotic resistance in the environment. Nat Rev Microbiol 20:257–269

    Article  CAS  PubMed  Google Scholar 

  • Lazzeri AM, Mangia NP, Mura ME, Floris I, Satta A, Ruiu L (2020) Potential of novel food-borne Lactobacillus isolates against the honeybee pathogen Paenibacillus larvae. Biocontrol Sci Tech 30:897–908

    Article  Google Scholar 

  • Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41:353–363

    Article  Google Scholar 

  • Lee YK, Salminen S (2009) Handbook of probiotics and prebiotics. John Wiley & Sons

  • Li C, Tang M, Li X, Zhou X (2022) Community dynamics in structure and function of honey bee gut bacteria in response to winter dietary shift. Am Soc Microbiol. https://doi.org/10.1128/mbio.01131-22

    Article  Google Scholar 

  • Lilly DM, Stillwell RH (1965) Probiotics: growth-promoting factors produced by microorganisms. Science 147:747–748

    Article  CAS  PubMed  Google Scholar 

  • López JH, Krainer S, Engert A, Schuehly W, Riessberger-Gallé U, Crailsheim K (2017) Sublethal pesticide doses negatively affect survival and the cellular responses in American foulbrood-infected honeybee larvae. Sci Rep 7:40853

    Article  PubMed  PubMed Central  Google Scholar 

  • Lourenço AP, Guidugli-Lazzarini KR, Freitas FC, Bitondi MM, Simões ZL (2013) Bacterial infection activates the immune system response and dysregulates microRNA expression in honey bees. Insect Biochem Mol Biol 43:474–482

    Article  PubMed  Google Scholar 

  • Ludvigsen J et al (2015) Shifts in the midgut/pyloric microbiota composition within a honey bee apiary throughout a season. Microbes Environ 30:235–244

    Article  PubMed  PubMed Central  Google Scholar 

  • Ludvigsen J, Andersen Å, Hjeljord L, Rudi K (2020) The honeybee gut mycobiota cluster by season versus the microbiota which cluster by gut segment. Veterinary Sciences 8:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Maes PW, Rodrigues PA, Oliver R, Mott BM, Anderson KE (2016) Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Mol Ecol 25:5439–5450

    Article  CAS  PubMed  Google Scholar 

  • 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 20:619–628

    Article  PubMed  Google Scholar 

  • Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78:2830–2840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirzaei R et al (2021) The emerging role of probiotics as a mitigation strategy against coronavirus disease 2019 (COVID-19). Adv Virol 166:1819–1840

    CAS  Google Scholar 

  • 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:e36393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morimoto T et al (2011) The habitat disruption induces immune-suppression and oxidative stress in honey bees. Ecol Evol 1:201–217

    Article  PubMed  PubMed Central  Google Scholar 

  • Muñoz-Atienza E et al (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  PubMed  Google Scholar 

  • Oldroyd BP (2007) What’s killing American honey bees? PLoS Biol 5:e168

    Article  PubMed  PubMed Central  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Ouwehand AC, Salminen S, Isolauri E (2002) Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 82:279–289

    Article  CAS  PubMed  Google Scholar 

  • Paris L, Roussel M, Pereira B, Delbac F, Diogon M (2017) Disruption of oxidative balance in the gut of the western honeybee Apis mellifera exposed to the intracellular parasite Nosema ceranae and to the insecticide fipronil. Microb Biotechnol 10:1702–1717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perdigon G, Maldonado Galdeano C (2017) Beneficial effect of probiotics consumption on the immune system. in: annals of nutrition and metabolism. Karger Allschwilerstrasse 10, CH-4009 Basel, Switzerland, pp 20–20

  • Perry J, Wright G (2013) The antibiotic resistance “mobilome”: searching for the link between environment and clinic. Front Microbiol 4:138

    Article  PubMed  PubMed Central  Google Scholar 

  • Pettis JS, Johnson J, Dively G (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99:153–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posada-Florez F et al (2019) Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Sci Rep 9:1–10

    Article  CAS  Google Scholar 

  • Powell JE, Martinson VG, Urban-Mead K, Moran NA (2014) Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl Environ Microbiol 80:7378–7387

    Article  PubMed  PubMed Central  Google Scholar 

  • Prosdocimi EM, Mapelli F, Gonella E, Borin S, Crotti E (2015) Microbial ecology-based methods to characterize the bacterial communities of non-model insects. J Microbiol Methods 119:110–125

    Article  PubMed  Google Scholar 

  • Rasic JL (1983) The role of dairy foods containing bifido-and acidophilus bacteria in nutrition and health? North Eur Dairy J 48:80–86

    Google Scholar 

  • Raymann K, Shaffer Z, Moran NA (2017) Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol 15:e2001861

    Article  PubMed  PubMed Central  Google Scholar 

  • Regulation E (2013) No 485/2013. Off J Eur Union 139:12–26

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 160:193–199

    Article  PubMed  Google Scholar 

  • Sabaté D, Cruz M, Benitez-Ahrendts M, Audisio M (2012) Beneficial effects of Bacillus subtilis subsp. subtilis Mori2, a honey-associated strain, on honeybee colony performance. Probiotics Antimicrob Proteins 4:39–46

    Article  PubMed  Google Scholar 

  • Salminen S et al (1998) Functional food science and gastrointestinal physiology and function. Br J Nutr 80:S147–S171

    Article  CAS  PubMed  Google Scholar 

  • Saraiva MA et al (2015) Relationship between honeybee nutrition and their microbial communities. Antonie Van Leeuwenhoek 107:921–933

    Article  CAS  PubMed  Google Scholar 

  • Schrezenmeir J, de Vrese M (2001) Probiotics, prebiotics, and synbiotics—approaching a definition–. Am J Clin Nutr 73:361s–364s

    Article  CAS  PubMed  Google Scholar 

  • Schwarz RS, Huang Q, Evans JD (2015) Hologenome theory and the honey bee pathosphere. Curr Opin Insect Sci 10:1–7

    Article  PubMed  Google Scholar 

  • Schwarz RS, Moran NA, Evans JD (2016) Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proc Natl Acad Sci 113:9345–9350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin SC et al (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334:670–674

    Article  CAS  PubMed  Google Scholar 

  • Smith EA et al (2021) Reclassification of seven honey bee symbiont strains as Bombella apis. BioRxiv. https://doi.org/10.1099/ijsem.0.004950

    Article  PubMed  PubMed Central  Google Scholar 

  • Smoragiewicz W, Bielecka M, Babuchowski A, Boutard A, Dubeau H (1993) Les probiotiques. Can J Microbiol 39:1089–1095

    Article  CAS  Google Scholar 

  • Soares KO, Oliveira CJBD, Rodrigues AE, Vasconcelos PC, Silva NMVD, Cunha Filho OGD, Madden C, Hale VL (2021) Tetracycline exposure alters key gut microbiota in Africanized honey bees (Apis mellifera scutellata x spp.). Front Ecol Evol. https://doi.org/10.3389/fevo.2021.716660

    Article  Google Scholar 

  • Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–652

    Article  PubMed  Google Scholar 

  • Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14:403–414

    Article  CAS  PubMed  Google Scholar 

  • Su Q et al (2022) Significant compositional and functional variation reveals the patterns of gut microbiota evolution among the widespread Asian honeybee populations. Front Microbiol. https://doi.org/10.3389/fmicb.2022.934459

    Article  PubMed  PubMed Central  Google Scholar 

  • Tarpy DR, Mattila HR, Newton IL (2015) Development of the honey bee gut microbiome throughout the queen-rearing process. Appl Environ Microbiol 81:3182–3191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Texts CAFHB (2001) Food and Agricultural Organization of the United Nations. World Health Organization, Rome:23–22.25

  • Tian B, Fadhil NH, Powell JE, Kwong WK, Moran NA (2012) Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees. Mbio 3:e00377-e1312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tola YH, Waweru JW, Hurst GD, Slippers B, Paredes JC (2020) Characterization of the Kenyan honey bee (Apis mellifera) gut microbiota: a first look at tropical and Sub-Saharan African bee associated microbiomes. Microorganisms 8:1721

  • Torres M, Brandan CP, Petroselli G, Erra-Balsells R, Audisio M (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  PubMed  Google Scholar 

  • Vásquez A et al (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE 7:e33188

    Article  PubMed  PubMed Central  Google Scholar 

  • Vojvodic S, Rehan SM, Anderson KE (2013) Microbial gut diversity of Africanized and European honey bee larval instars. PLoS ONE 8:e72106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K et al (2021) Gut microbiota protects honey bees (Apis mellifera L.) against polystyrene microplastics exposure risks. J Hazard Mater 402:123828

    Article  CAS  PubMed  Google Scholar 

  • Williams GR, Sampson MA, Shutler D, Rogers RE (2008) Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? J Invertebr Pathol 99:342–344

    Article  CAS  PubMed  Google Scholar 

  • Winfree R, Williams NM, Gaines H, Ascher JS, Kremen C (2008) Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. J Appl Ecol 45:793–802

    Article  Google Scholar 

  • Yeung T et al (2006) Receptor activation alters inner surface potential during phagocytosis. Science 313:347–351

    Article  CAS  PubMed  Google Scholar 

  • Yoshiyama M, Kimura K (2009) Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J Invertebr Pathol 102:91–96

    Article  PubMed  Google Scholar 

  • 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 Invertebr Pathol 112:62–67

    Article  CAS  PubMed  Google Scholar 

  • Zendo T, Ohashi C, Maeno S, Piao X, Salminen S, Sonomoto K, Endo A (2020) Kunkecin A, a new nisin variant bacteriocin produced by the fructophilic lactic acid bacterium, Apilactobacillus kunkeei FF30-6 isolated from honey bees. Front Microbiol 11:571903

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA (2017) Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci 114:4775–4780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng H, Steele MI, Leonard SP, Motta EV, Moran NA (2018) Honey bees as models for gut microbiota research. Lab Anim 47:317–325

    Article  Google Scholar 

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KA conceived the idea, performed literature search and wrote the review. MBS edited the manuscript, and MBS, EC, ASM and AC finalized it.

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Correspondence to Khaoula Abdi.

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Abdi, K., Ben Said, M., Crotti, E. et al. The promise of probiotics in honeybee health and disease management. Arch Microbiol 205, 73 (2023). https://doi.org/10.1007/s00203-023-03416-z

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