Selection of Probiotics for Honey Bees: The In Vitro Inhibition of Paenibacillus larvae, Melissococcus plutonius, and Serratia marcescens Strain Sicaria by Host-Specific Lactobacilli and Bifidobacteria

. 2025 May 20 ; 13 (5) : . [epub] 20250520

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40431330

Grantová podpora
QK21010088 CZECH NATIONAL AGRICULTURAL RESEARCH AGENCY
Project No. LM2023064 METROFOOD-CZ Research Infrastructure (https://metrofood.cz), supported by the Ministry of Education, Youth and Sports of the Czech Republic

Odkazy

PubMed 40431330
PubMed Central PMC12113734
DOI 10.3390/microorganisms13051159
PII: microorganisms13051159
Knihovny.cz E-zdroje

Host-specific Lactobacillus and Bifidobacterium species constitute the core microbiota of the honey bee digestive tract and are recognized for their probiotic properties. One of the properties of these bacteria is the inhibition of bacterial pathogens such as Paenibacillus larvae and Melissococcus plutonius, the causative agents of American and European foulbrood, respectively. Additionally, Serratia marcescens has emerged as a relevant opportunistic pathogen. Although several previously published studies have examined the inhibition of selected bacterial pathogens of bees by members of the bee physiological microbiota, none have simultaneously investigated the inhibition of multiple clinical isolates of P. larvae, M. plutonius, and S. marcescens using a wide range of bifidobacterial and lactobacilli strains isolated from various locations within a single country. Thus, this study evaluated the antimicrobial potential of Lactobacillus and Bifidobacterium strains against these pathogens, with a focus on strain-dependent inhibition. A total of 111 bacterial strains (62 Lactobacillus and 49 Bifidobacterium) were isolated from the digestive tracts of honey bees collected from eight sites across the Czech Republic. Using 16S rRNA gene sequencing, the isolates were classified and tested in vitro against four P. larvae isolates, one M. plutonius isolate, and the S. marcescens strain sicaria in modified BHI medium. Twenty-eight strains (~26%) exhibited strong inhibition (≥21 mm) against at least two P. larvae isolates, while 12 strains showed moderate inhibition (16-20 mm) against all four isolates. Inhibition of M. plutonius and S. marcescens was observed in three and twenty strains, respectively. The most effective strains belonged to Bifidobacterium asteroides, B. choladohabitans, B. polysaccharolyticum, Lactobacillus apis, L. helsingborgensis, L. kullabergensis, and L. melliventris. These results underscore the strain-dependent nature of antimicrobial activity and highlight the importance of selecting probiotic strains with broad-spectrum pathogen inhibition to support honey bee health.

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Alberoni D., Gaggìa F., Baffoni L., Modesto M.M., Biavati B., Di Gioia D. Bifidobacterium Xylocopae sp. nov. and Bifidobacterium Aemilianum sp. nov., from the Carpenter Bee (Xylocopa Violacea) Digestive Tract. Syst. Appl. Microbiol. 2019;42:205–216. doi: 10.1016/j.syapm.2018.11.005. PubMed DOI

Chen J., Wang J., Zheng H. Characterization of Bifidobacterium Apousia sp. nov., Bifidobacterium Choladohabitans sp. nov., and Bifidobacterium Polysaccharolyticum sp. nov., Three Novel Species of the Genus Bifidobacterium from Honeybee Gut. Syst. Appl. Microbiol. 2021;44:126247. doi: 10.1016/j.syapm.2021.126247. PubMed DOI

Engel P., Kwong W.K., Moran N.A. Frischella Perrara gen. nov., sp. nov., a Gammaproteobacterium Isolated from the Gut of the Honeybee, Apis Mellifera. Int. J. Syst. Evol. Microbiol. 2013;63:3646–3651. doi: 10.1099/ijs.0.049569-0. PubMed DOI

Killer J., Dubná S., Sedláček I., Švec P. Lactobacillus Apis sp. nov., from the Stomach of Honeybees (Apis mellifera), Having an in vitro Inhibitory Effect on the Causative Agents of American and European Foulbrood. Int. J. Syst. Evol. Microbiol. 2014;64:152–157. doi: 10.1099/ijs.0.053033-0. PubMed DOI

Killer J., Kopečný J., Mrázek J., Havlík J., Koppová I., Benada O., Rada V., Kofroňová O. Bombiscardovia Coagulans gen. nov., sp. nov., a New Member of the Family Bifidobacteriaceae Isolated from the Digestive Tract of Bumblebees. Syst. Appl. Microbiol. 2010;33:359–366. doi: 10.1016/j.syapm.2010.08.002. PubMed DOI

Killer J., Votavová A., Valterová I., Vlková E., Rada V., Hroncová Z. Lactobacillus Bombi sp. nov., from the Digestive Tract of Laboratory-Reared Bumblebee Queens (Bombus Terrestris) Int. J. Syst. Evol. Microbiol. 2014;64:2611–2617. doi: 10.1099/ijs.0.063602-0. PubMed DOI

Kwong W.K., Moran N.A. 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. 2013;63:2008–2018. doi: 10.1099/ijs.0.044875-0. PubMed DOI

Olofsson T.C., Alsterfjord M., Nilson B., Butler È., Vásquez A. 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. 2014;64:3109–3119. doi: 10.1099/ijs.0.059600-0. PubMed DOI PMC

Olofsson T.C., Modesto M., Pascarelli S. Bifidobacterium Mellis sp. nov., Isolated from the Honey Stomach of the Honey Bee Apis mellifera. Int. J. Syst. Evol. Microbiol. 2023;73:3. doi: 10.1099/ijsem.0.005766. PubMed DOI

Kešnerová L., Mars R.A.T., Ellegaard K.M., Troilo M., Sauer U., Engel P. Disentangling Metabolic Functions of Bacteria in the Honey Bee Gut. PLoS Biol. 2017;15:e2003467. doi: 10.1371/journal.pbio.2003467. PubMed DOI PMC

Motta E.V.S., Gage A., Smith T.E., Blake K.J., Kwong W.K., Riddington I.M., Moran N.A. Host-Microbiome Metabolism of a Plant Toxin in Bees. Elife. 2022;11:e82595. doi: 10.7554/eLife.82595. PubMed DOI PMC

Zheng H., Perreau J., Elijah Powell J., Han B., Zhang Z., Kwong W.K., Tringe S.G., Moran N.A. Division of Labor in Honey Bee Gut Microbiota for Plant Polysaccharide Digestion. Proc. Natl. Acad. Sci. USA. 2019;116:25909–25916. doi: 10.1073/pnas.1916224116. PubMed DOI PMC

Leska A., Nowak A., Miśkiewicz K., Rosicka-Kaczmarek J. Binding and Detoxification of Insecticides by Potentially Probiotic Lactic Acid Bacteria Isolated from Honeybee (Apis mellifera L.) Environment—An In Vitro Study. Cells. 2022;11:3743. doi: 10.3390/cells11233743. PubMed DOI PMC

Liu P., Niu J., Zhu Y., Li Z., Ye L., Cao H., Shi T., Yu L. Apilactobacillus kunkeei Alleviated Toxicity of Acetamiprid in Honeybee. Insects. 2022;13:1167. doi: 10.3390/insects13121167. PubMed DOI PMC

Nowak A., Szczuka D., Górczyńska A., Motyl I., Kręgiel D. Characterization of Apis Mellifera Gastrointestinal Microbiota and Lactic Acid Bacteria for Honeybee Protection-A Review. Cells. 2021;10:701. doi: 10.3390/cells10030701. PubMed DOI PMC

Smriti, Rana A., Singh G., Gupta G. Prospects of Probiotics in Beekeeping: A Review for Sustainable Approach to Boost Honeybee Health. Arch. Microbiol. 2024;206:205. doi: 10.1007/s00203-024-03926-4. PubMed DOI

Garrido P.M., Porrini M.P., Alberoni D., Baffoni L., Scott D., Mifsud D., Eguaras M.J., Di Gioia D. Beneficial Bacteria and Plant Extracts Promote Honey Bee Health and Reduce Nosema Ceranae Infection. Probiotics Antimicrob. Proteins. 2024;16:259–274. doi: 10.1007/s12602-022-10025-7. PubMed DOI PMC

Janashia I., Alaux C. Specific Immune Stimulation by Endogenous Bacteria in Honey Bees (Hymenoptera: Apidae) J. Econ. Entomol. 2016;109:1474–1477. doi: 10.1093/jee/tow065. PubMed DOI

Ye M., Li X., Yang F., Zhou B. Beneficial Bacteria as Biocontrol Agents for American Foulbrood Disease in Honey Bees (Apis mellifera) J. Insect Sci. 2023;23:6. doi: 10.1093/jisesa/iead013. PubMed DOI PMC

Zheng H., Powell J.E., Steele M.I., Dietrich C., Moran N.A. Honeybee Gut Microbiota Promotes Host Weight Gain via Bacterial Metabolism and Hormonal Signaling. Proc. Natl. Acad. Sci. USA. 2017;114:4775–4780. doi: 10.1073/pnas.1701819114. PubMed DOI PMC

Alberoni D., Baffoni L., Gaggìa F., Ryan P.M., Murphy K. Impact of Beneficial Bacteria Supplementation on the Gut Microbiota, Colony Development and Productivity of Apis mellifera L. Benef. Microbes. 2018;9:269–278. doi: 10.3920/BM2017.0061. PubMed DOI

Anderson K.E., Ricigliano V.A., Mott B.M., Copeland D.C., Floyd A.S., Maes P. The Queen’s Gut Refines with Age: Longevity Phenotypes in a Social Insect Model. Microbiome. 2018;6:108. doi: 10.1186/s40168-018-0489-1. PubMed DOI PMC

Wang H., Lei L., Chen W., Chi X., Han K., Wang Y., Ma L., Liu Z., Xu B. The Comparison of Antioxidant Performance, Immune Performance, IIS Activity and Gut Microbiota Composition between Queen and Worker Bees Revealed the Mechanism of Different Lifespan of Female Casts in the Honeybee. Insects. 2022;13:772. doi: 10.3390/insects13090772. PubMed DOI PMC

Janashia I., Choiset Y., Jozefiak D., Déniel F., Coton E., Moosavi-Movahedi A.A., Chanishvili N., Haertlé T. Beneficial Protective Role of Endogenous Lactic Acid Bacteria against Mycotic Contamination of Honeybee Beebread. Probiotics Antimicrob. Proteins. 2018;10:638–646. doi: 10.1007/s12602-017-9379-2. PubMed DOI

Daisley B.A., Pitek A.P., Chmiel J.A., Gibbons S., Chernyshova A.M., Al K.F., Faragalla K.M., Burton J.P., Thompson G.J., Reid G. Lactobacillus spp. Attenuate Antibiotic-Induced Immune and Microbiota Dysregulation in Honey Bees. Commun. Biol. 2020;3:534. doi: 10.1038/s42003-020-01259-8. PubMed DOI PMC

Powell J.E., Carver Z., Leonard S.P., Moran N.A. Field-Realistic Tylosin Exposure Impacts Honey Bee Microbiota and Pathogen Susceptibility, Which Is Ameliorated by Native Gut Probiotics. Microbiol. Spectr. 2021;9:e0010321. doi: 10.1128/Spectrum.00103-21. PubMed DOI PMC

Wu J., Lang H., Mu X., Zhang Z., Su Q., Hu X., Zheng H. Honey Bee Genetics Shape the Strain-Level Structure of Gut Microbiota in Social Transmission. Microbiome. 2021;9:225. doi: 10.1186/s40168-021-01174-y. PubMed DOI PMC

Zhang Z., Mu X., Cao Q., Shi Y., Hu X., Zheng H. Honeybee Gut Lactobacillus Modulates Host Learning and Memory Behaviors via Regulating Tryptophan Metabolism. Nat. Commun. 2022;13:2037. doi: 10.1038/s41467-022-29760-0. PubMed DOI PMC

Vernier C.L., Nguyen L.A., Gernat T., Ahmed A.C., Chen Z., Robinson G.E. Gut Microbiota Contribute to Variations in Honey Bee Foraging Intensity. ISME J. 2024;18:wrae030. doi: 10.1093/ismejo/wrae030. PubMed DOI PMC

Forsgren E., Olofsson T.C., Vásquez A., Fries I. Novel Lactic Acid Bacteria Inhibiting Paenibacillus Larvae in Honey Bee Larvae Novel Lactic Acid Bacteria Inhibiting Paenibacillus Larvae in Honey Bee Larvae. Apidologie. 2010;41:99–108. doi: 10.1051/apido/2009065. DOI

Iorizzo M., Ganassi S., Albanese G., Letizia F., Testa B., Tedino C., Petrarca S., Mutinelli F., Mazzeo A., De Cristofaro A. Antimicrobial Activity from Putative Probiotic Lactic Acid Bacteria for the Biological Control of American and European Foulbrood Diseases. Vet. Sci. 2022;9:236. doi: 10.3390/vetsci9050236. PubMed DOI PMC

Lang H., Duan H., Wang J., Zhang W., Guo J., Zhang X., Hu X., Zheng H. Specific Strains of Honeybee Gut Lactobacillus Stimulate Host Immune System to Protect against Pathogenic Hafnia Alvei. Microbiol. Spectr. 2022;23:e0189621. doi: 10.1128/spectrum.01896-21. PubMed DOI PMC

Truong A.T., Kang J.E., Yoo M.S., Nguyen T.T., Youn S.Y., Yoon S.S., Cho Y.S. Probiotic Candidates for Controlling Paenibacillus Larvae, a Causative Agent of American Foulbrood Disease in Honey Bee. BMC Microbiol. 2023;23:150. doi: 10.1186/s12866-023-02902-0. PubMed DOI PMC

Wu M., Sugimura Y., Takaya N., Takamatsu D., Kobayashi M., Taylor D.M., Yoshiyama M. Characterization of Bifidobacteria in the Digestive Tract of the Japanese Honeybee, Apis Cerana Japonica. J. Invertebr. Pathol. 2013;112:88–93. doi: 10.1016/j.jip.2012.09.005. PubMed DOI

Zeid A.A.A., Khattaby A.M., El-Khair I.A.A., Gouda H.I.A. Detection Bioactive Metabolites of Fructobacillus Fructosus strain HI-1 Isolated from Honey Bee’s Digestive Tract Against Paenibacillus Larvae. Probiotics Antimicrob. Proteins. 2022;14:476–485. doi: 10.1007/s12602-021-09812-5. PubMed DOI

Arredondo D., Castelli L., Porrini M.P., Garrido P.M., Eguaras M.J., Zunino P., Antúnez K. Lactobacillus Kunkeei Strains Decreased the Infection by Honey Bee Pathogens Paenibacillus Larvae and Nosema Ceranae. Benef. Microbes. 2018;9:279–290. doi: 10.3920/BM2017.0075. PubMed DOI

Baffoni L., Gaggìa F., Alberoni D., Cabbri R., Nanetti A., Biavati B., Di Gioia D. Effect of Dietary Supplementation of Bifidobacterium and Lactobacillus Strains in Apis Mellifera L. Against Nosema ceranae. Benef. Microbes. 2016;7:45–51. doi: 10.3920/BM2015.0085. PubMed DOI

Iorizzo M., Lombardi S.J., Ganassi S., Testa B., Ianiro M., Letizia F., Succi M., Tremonte P., Vergalito F., Cozzolino A., et al. Antagonistic Activity against Ascosphaera apis and Functional Properties of Lactobacillus kunkeei Strains. Antibiotics. 2020;9:262. doi: 10.3390/antibiotics9050262. PubMed DOI PMC

Tejerina M.R., Cabana M.J., Benitez-Ahrendts M.R. Strains of Lactobacillus spp. Reduce Chalkbrood in Apis mellifera. J. Invertebr. Pathol. 2021;178:107521. doi: 10.1016/j.jip.2020.107521. PubMed DOI

Brar G., Ngor L., McFrederick Q.S., Torson A.S., Rajamohan A., Rinehart J., Singh P., Bowsher J.H. High Abundance of Lactobacilli in the Gut Microbiome of Honey Bees During Winter. Sci. Rep. 2025;15:7409. doi: 10.1038/s41598-025-90763-0. PubMed DOI PMC

Reid G., Gadir A.A., Dhir R. Probiotics: Reiterating What They Are and What They Are Not. Front. Microbiol. 2019;10:424. doi: 10.3389/fmicb.2019.00424. PubMed DOI PMC

Endo A., Salminen S. Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Syst. Appl. Microbiol. 2013;36:444–448. doi: 10.1016/j.syapm.2013.06.002. PubMed DOI

Vásquez A., Olofsson T.C., Forsgren E., Fries I., Paxton R.J., Flaberg E., Szekely L., Odham G. Symbionts as major modulators of insect health: Lactic acid bacteria and honeybees. PLoS ONE. 2012;7:e33188. doi: 10.1371/annotation/3ac2b867-c013-4504-9e06-bebf3fa039d1. PubMed DOI PMC

Killer J., Kopečný J., Mrázek J., Rada V., Dubná S., Marounek M. Bifidobacteria in the Digestive Tract of Bumblebees. Anaerobe. 2010;16:165–170. doi: 10.1016/j.anaerobe.2009.07.007. PubMed DOI

Matiašovic J., Bzdil J., Papežíková I., Čejková D., Vasina E., Bizos J., Navrátil S., Šedivá M., Klaudiny J., Pikula J. Genomic Analysis of Paenibacillus larvae Isolates from the Czech Republic and the Neighbouring Regions of Slovakia. Res. Vet. Sci. 2023;158:34–40. doi: 10.1016/j.rvsc.2023.03.007. PubMed DOI

Thebeau J.M., Liebe D., Masood F., Kozii I.V., Klein C.D., Zabrodski M.W., Moshynskyy I., Sobchishin L., Wilson G., Guarna M.M., et al. Article Investigation of Melissococcus Plutonius Isolates from 3 Outbreaks of European Foulbrood Disease in Commercial Beekeeping Operations in Western Canada. Can. Vet. J. 2022;63:935–942. PubMed PMC

Burritt N.L., Foss N.J., Neeno-Eckwall E.C., Church J.O., Hilger A.M., Hildebrand J.A., Warshauer D.M., Perna N.T., Burritt J.B. Sepsis and Hemocyte Loss in Honey Bees (Apis Mellifera) Infected with Serratia Marcescens Strain Sicaria. PLoS ONE. 2016;11:e0167752. doi: 10.1371/journal.pone.0167752. PubMed DOI PMC

Forster R.J., Teather R.M., Gong J., Deng S.J. 16S rDNA Analysis of Butyrivibrio Fibrisolvens: Phylogenetic Position and Relation to Butyrate-Producing Anaerobic Bacteria from the Rumen of White-Tailed Deer. Lett. Appl. Microbiol. 1996;23:218–222. doi: 10.1111/j.1472-765X.1996.tb00069.x. PubMed DOI

Galkiewicz J.P., Kellogg C.A. Cross-Kingdom Amplification Using Bacteria-Specific Primers: Complications for Studies of Coral Microbial Ecology. Appl Environ Microbiol. 2008;74:7828–7831. doi: 10.1128/AEM.01303-08. PubMed DOI PMC

Killer J., Mekadim C., Pechar R., Bunešová V., Mrázek J., Vlková E. Gene Encoding the CTP Synthetase as an Appropriate Molecular Tool for Identification and Phylogenetic Study of the Family Bifidobacteriaceae. Microbiologyopen. 2018;7:e00579. doi: 10.1002/mbo3.579. PubMed DOI PMC

Cheng L., Kiewiet M.B.G., Logtenberg M.J., Groeneveld A., Nauta A., Schols H.A., Walvoort M.T.C., Harmsen H.J.M., de Vos P. Effects of Different Human Milk Oligosaccharides on Growth of Bifidobacteria in Monoculture and Co-Culture with Faecalibacterium Prausnitzii. Front. Microbiol. 2020;11:569700. doi: 10.3389/fmicb.2020.569700. PubMed DOI PMC

Killer J., Havlík J., Bunešová V., Vlková E., Benada O. Pseudoscardovia radai sp. nov., A Representative of the Family Bifidobacteriaceae Isolated from the Digestive Tract of a Wild Pig (Sus Scrofa Scrofa) Int. J. Syst. Evol. Microbiol. 2014;64:2932–2938. doi: 10.1099/ijs.0.063230-0. PubMed DOI

Chun J., Oren A., Ventosa A., Christensen H., Arahal D.R., da Costa M.S., Rooney A.P., Yi H., Xu X.W., De Meyer S., et al. Proposed Minimal Standards for the Use of Genome Data for the Taxonomy of Prokaryotes. Int. J. Syst. Evol. Microbiol. 2018;68:461–466. doi: 10.1099/ijsem.0.002516. PubMed DOI

Ellegaard K.M., Tamarit D., Javelind E., Olofsson T.C., Andersson S.G.E., Vásquez A. Extensive Intra-Phylotype Diversity in Lactobacilli and Bifidobacteria from the Honeybee Gut. BMC Genom. 2015;16:284. doi: 10.1186/s12864-015-1476-6. PubMed DOI PMC

Heyndrickx M., Vandemeulebroecke K., Hoste B. Reclassification of Paenibacillus (Formerly Bacillus) Pulvifaciens (Nakamura 1984) Ash et al. 1994, a Later Subjective Synonym of Paenibacillus (Formerly Bacillus) larvae (White 1906) Ash et al. 1994, as a Subspecies of P. Larvae, with Emended Descriptions of P. Larvae as P. Larvae subs P. Larvae and P. Larvae subsp. Pulvifaciens. Int. J. Syst. Bacteriol. 1996;46:270–279. doi: 10.1099/00207713-46-1-270. PubMed DOI

Fijan S. Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature. Int. J. Environ. Res. Public Health. 2014;11:4745–4767. doi: 10.3390/ijerph110504745. PubMed DOI PMC

Hejazi A., Falkiner F.R. Serratia marcescens. J. Med. Microbiol. 1997;46:903–912. doi: 10.1099/00222615-46-11-903. PubMed DOI

Raymann K., Coon K.L., Shaffer Z., Salisbury S., Moran N.A. Pathogenicity of Serratia marcescens Strains in Honey Bees. mBio. 2018;9:e01649-18. doi: 10.1128/mBio.02855-18. Erratum in mBio 2019, 10, e02855-18. PubMed DOI PMC

Ansari M.J., Al-Ghamdi A., Nuru A., Ahmed A.M., Ayaad T.H., Al-Qarni A., Alattal Y., Al-Waili N. Survey and Molecular Detection of Melissococcus plutonius, the Causative Agent of European Foulbrood in Honeybees in Saudi Arabia. Saudi J. Biol. Sci. 2017;24:1327–1335. doi: 10.1016/j.sjbs.2016.10.012. PubMed DOI PMC

Daisley B.A., Pitek A.P., Chmiel J.A., Al K.F., Chernyshova A.M., Faragalla K.M., Burton J.P., Thompson G.J., Reid G. Novel Probiotic Approach to Counter Paenibacillus larvae Infection in Honey Bees. ISME J. 2020;14:476–491. doi: 10.1038/s41396-019-0541-6. PubMed DOI PMC

Butler È., Alsterfjord M., Olofsson T.C., Karlsson C., Malmström J., Vásquez A. Proteins of Novel Lactic Acid Bacteria from Apis mellifera mellifera: An Insight into the Production of Known Extra-Cellular Proteins during Microbial Stress. BMC Microbiol. 2013;13:235. doi: 10.1186/1471-2180-13-235. PubMed DOI PMC

Masood F., Thebeau J.M., Cloet A., Kozii I.V., Zabrodski M.W., Biganski S., Wood S.C. Evaluating approved and alternative treatments against an oxytetracycline-resistant bacterium responsible for European foulbrood disease in honey bees. Sci. Rep. 2022;12:5906. doi: 10.1038/s41598-022-09796-4. PubMed DOI PMC

Daisley B.A., Pitek A.P., Mallory E., Chernyshova A.M., Allen-Vercoe E., Reid G., Thompson G.J. Disentangling the microbial ecological factors impacting honey bee susceptibility to Paenibacillus larvae infection. Trends Microbiol. 2023;31:521–534. doi: 10.1016/j.tim.2022.11.012. PubMed DOI

Iorizzo M., Testa B., Lombardi S.J., Ganassi S., Ianiro M., Letizia F., De Cristofaro A. Antimicrobial activity against Paenibacillus larvae and functional properties of Lactiplantibacillus plantarum strains: Potential benefits for honeybee health. Antibiotics. 2020;9:442. doi: 10.3390/antibiotics9080442. PubMed DOI PMC

Borges D., Guzman-Novoa E., Goodwin P.H. Effects of prebiotics and probiotics on honey bees (Apis mellifera) infected with the microsporidian parasite Nosema ceranae. Microorganisms. 2021;9:481. doi: 10.3390/microorganisms9030481. PubMed DOI PMC

Mallory E., Freeze G., Daisley B.A., Allen-Vercoe E. Revisiting the role of pathogen diversity and microbial interactions in honeybee susceptibility and treatment of Melissococcus plutonius infection. Front. Vet. Sci. 2024;11:1495010. doi: 10.3389/fvets.2024.1495010. PubMed DOI PMC

Toutiaee S., Mojgani N., Harzandi N., Moharrami M., Mokhberosafa L. In vitro probiotic and safety attributes of Bacillus spp. isolated from beebread, honey samples and digestive tract of honeybees Apis mellifera. Lett. Appl. Microbiol. 2022;74:656–665. doi: 10.1111/lam.13650. PubMed DOI

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