Skip to main content
SpringerLink
Log in

Secondary Metabolites Produced by Honey Bee-Associated Bacteria for Apiary Health: Potential Activity of Platynecine

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Secondary metabolites of bacteria associated with honey bees were evaluated as part of an investigation on their potentiality for apiary health. Low molecular weight compounds released into culture filtrates by the four bacterial isolates taken from surface of healthy honey bees were analyzed using time-of-flight mass spectrometry. Only one low molecular weight compound was found in the culture filtrate of each isolate. Bacillus thuringiensis, Bifidobacterium asteroides and Acetobacteraceae bacterium, released into culture filtrates platynecine, a pyrrolizidine alkaloid of plant origin, which, until now, had never been reported as produced by bacteria. Lactobacillus kunkeei produced a 3,5-dinitropyridine, of unknown biological action never associated so far to bacteria. The highest relative concentration of platynecine was detected in B. thuringiensis (100%), B. asteroides and A. bacterium showed a concentration above 50% and below 25% that concentration. An in vitro assay on the potential for controlling the parasitic mite Varroa destructor by the culture filtrates of the three platynecine-producing bacteria was performed. Varroa mite mortality was proportional to the platynecine relative concentration into culture filtrate. Although miticidal activity of B. thuringiensis might be associated to other toxic proteins produced by this species, B. asteroides toxicity toward V. destructor along with the other findings of this study support the hypothesis that platynecine plays a direct or an indirect role in controlling varroa. Findings of this study suggest that secondary metabolites released by honey bee-associated bacteria represent a source of natural compounds to be considered in the challenge for counteracting the colony decline.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Source: https://www.chemspider.com/Chemical-Structure.83763.html. Features in Table 2

Fig. 2

Similar content being viewed by others

References

  1. Smith KM, Loh EH, Rostal MK, Zambrana-Torrelio CM, Mendiola L, Daszak P (2013) Pathogens, pests, and economics: drivers of honey bee colony declines and losses. EcoHealth 10:434–445. https://doi.org/10.1007/s10393-013-0870-2

    Article  PubMed  Google Scholar 

  2. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007

    Article  PubMed  Google Scholar 

  3. 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 Invertebr Pathol 103(Suppl 1):S80–95. https://doi.org/10.1016/j.jip.2009.06.011

    Article  PubMed  Google Scholar 

  4. New TR (2016) Alien species and insect conservation. https://doi.org/10.1007/978-3-319-38774-1

  5. Chen YP, Siede R (2007) Honey bee viruses. Adv Virus Res 70:33–80. https://doi.org/10.1016/S0065-3527(07)70002-7

    Article  PubMed  CAS  Google Scholar 

  6. Ramsey SD, Ochoa R, Bauchan G, Gulbronson C, Mowery JD, Cohen A, Lim D, Joklik J, Cicero JM, Ellis JD, Hawthorne D, vanEngelsdorp D (2019) Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc Natl Acad Sci USA 116:1792–1801. https://doi.org/10.1073/pnas.1818371116

    Article  PubMed  CAS  Google Scholar 

  7. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103(Suppl):S96–119. https://doi.org/10.1016/j.jip.2009.07.016

    Article  PubMed  Google Scholar 

  8. Currie RW, Pernal SF, Guzmán-Novoa E (2010) Honey bee colony losses in Canada. J Apic Res 49:104–106. https://doi.org/10.3896/IBRA.1.49.1.18

    Article  Google Scholar 

  9. Rademacher E, Imdorf A (2004) Legalization of the use of oxalic acid in varroa control. Bee World 85:70–72. https://doi.org/10.1080/0005772X.2004.11099633

    Article  Google Scholar 

  10. Charrière J-D, Imdorf A (2002) Oxalic acid treatment by trickling against Varroa destructor: recommendations for use in central Europe and under temperate climate conditions. Bee World 83:51–60. https://doi.org/10.1080/0005772X.2002.11099541

    Article  Google Scholar 

  11. Cimmino A, Freda F, Santoro E, Superchi S, Evidente A, Cristofaro M, Masi M (2019) alpha-Costic acid, a plant sesquiterpene with acaricidal activity against Varroa destructor parasitizing the honey bee. Nat Prod Res. https://doi.org/10.1080/14786419.2019.1652291

    Article  PubMed  Google Scholar 

  12. Shaw KE, Davidson G, Clark SJ, Ball BV, Pell JK, Chandler D, Sunderland KD (2002) Laboratory bioassays to assess the pathogenicity of mitosporic fungi to Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of the honeybee, Apis mellifera. Biol Control 24:266–276. https://doi.org/10.1016/S1049-9644(02)00029-4

    Article  Google Scholar 

  13. Lodesani M, Costa C, Franceschetti S, Bergomi P, Galaverna G, Dall’Asta C (2017) Toxicity of destruxins against the parasitic mite Varroa destructor and its host Apis mellifera. J Apic Res 56:278–287. https://doi.org/10.1080/00218839.2017.1304611

    Article  Google Scholar 

  14. Meikle WG, Sammataro D, Neumann P, Pflugfelder J (2012) Challenges for developing pathogen-based biopesticides against Varroa destructor (Mesostigmata: Varroidae). Apidologie 43:501–514. https://doi.org/10.1007/s13592-012-0118-0

    Article  Google Scholar 

  15. Tu S, Qiu X, Cao L, Han R, Zhang Y, Liu X (2010) Expression and characterization of the chitinases from Serratia marcescens GEI strain for the control of Varroa destructor, a honey bee parasite. J Invertebr Pathol 104:75–82. https://doi.org/10.1016/j.jip.2010.02.002

    Article  PubMed  CAS  Google Scholar 

  16. Alquisira-Ramírez EV, Peña-Chora G, Hernández-Velázquez VM, Alvear-García A, Arenas-Sosa I, Suarez-Rodríguez R (2017) Effects of Bacillus thuringiensis strains virulent to Varroa destructor on larvae and adults of Apis mellifera. Ecotoxicol Environ Saf 142:69–78. https://doi.org/10.1016/j.ecoenv.2017.03.050

    Article  PubMed  CAS  Google Scholar 

  17. Tsagou V, Lianou A, Lazarakis D, Emmanouel N, Aggelis G (2004) Newly isolated bacterial strains belonging to Bacillaceae (Bacillus sp.) and Micrococcaceae accelerate death of the honey bee mite, Varroa destructor (V. jacobsoni), in laboratory assays. Biotechnol Lett 26:529–532. https://doi.org/10.1023/B:BILE.0000019563.92959.0e

    Article  PubMed  CAS  Google Scholar 

  18. Sabaté DC, Cruz MS, Benitez-Ahrendts MR, Audisio MC (2012) Beneficial effects of Bacillus subtilis subsp. subtilis Mori2, a honey-associated strain, on honeybee colony performance. Probiotics Antimicrobial Proteins 4:39–46. https://doi.org/10.1007/s12602-011-9089-0

    Article  PubMed  Google Scholar 

  19. Audisio MC, Sabaté DC, Benítez-Ahrendts MR (2015) Effect of Lactobacillus johnsonii CRL1647 on different parameters of honeybee colonies and bacterial populations of the bee gut. Beneficial Microbes 6:687–695. https://doi.org/10.3920/BM2014.0155

    Article  PubMed  CAS  Google Scholar 

  20. Crotti E, Balloi A, Hamdi C, Sansonno L, Marzorati M, Gonella E, Favia G, Cherif A, Bandi C, Alma A, Daffonchio D (2012) Microbial symbionts: a resource for the management of insect-related problems. Microb Biotechnol 5:307–317. https://doi.org/10.1111/j.1751-7915.2011.00312.x

    Article  PubMed  PubMed Central  Google Scholar 

  21. Olofsson TC, Butler E, Markowicz P, Lindholm C, Larsson L, Vasquez A (2014) Lactic acid bacterial symbionts in honeybees—an unknown key to honey’s antimicrobial and therapeutic activities. Int Wound J 13:668–679. https://doi.org/10.1111/iwj.12345

    Article  PubMed  Google Scholar 

  22. Beemelmanns C, Guo H, Rischer M, Poulsen M (2016) Natural products from microbes associated with insects. Beilstein J Org Chem 12:314–327

    Article  CAS  Google Scholar 

  23. Crawford JM, Clardy J (2011) Bacterial symbionts and natural products. Chem Commun (Camb) 47:7559–7566. https://doi.org/10.1039/c1cc11574j

    Article  CAS  Google Scholar 

  24. Schmidt EW (2008) Trading molecules and tracking targets in symbiotic interactions. Nat Chem Biol 4:466–473. https://doi.org/10.1038/nchembio.101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  26. Rampersad J, Khan A, Ammons D (2002) Usefulness of staining parasporal bodies when screening for Bacillus thuringiensis. J Invertebr Pathol 79:203–204. https://doi.org/10.1016/S0022-2011(02)00018-6

    Article  PubMed  Google Scholar 

  27. Kim S, Thiessen PA, Bolton EE, Chen J, Fu G, Gindulyte A, Han L, He J, He S, Shoemaker BA, Wang J, Yu B, Zhang J, Bryant SH (2016) PubChem substance and compound databases. Nucleic Acids Res 44:D1202–D1213. https://doi.org/10.1093/nar/gkv951

    Article  PubMed  CAS  Google Scholar 

  28. Kleinbaum DG, Klein M (2012) Survival analysis. A self-learning text, 3rd edn. Springer-Verlag, New York. https://doi.org/10.1007/978-1-4419-6646-9

    Google Scholar 

  29. Moreira R, Pereira MD, Valentão P, Andrade BP (2018) Pyrrolizidine alkaloids: chemistry, pharmacology, toxicology and food safety. Int J Mol Sci. https://doi.org/10.3390/ijms19061668

    Article  PubMed  PubMed Central  Google Scholar 

  30. Winkler M, Cakir B, Sander W (2004) 3,5-Pyridyne—a heterocyclic meta-benzyne derivative. J Am Chem Soc 126:6135–6149. https://doi.org/10.1021/ja039142u

    Article  PubMed  CAS  Google Scholar 

  31. Schoning V, Hammann F, Peinl M, Drewe J (2017) Editor’s highlight: identification of any structure-specific hepatotoxic potential of different pyrrolizidine alkaloids using random forests and artificial neural networks. Toxicol Sci 160:361–370. https://doi.org/10.1093/toxsci/kfx187

    Article  PubMed  CAS  Google Scholar 

  32. Hartmann T, Ober D (2000) Biosynthesis and metabolism of pyrrolizidine alkaloids in plants and specialized insect herbivores. In: Leeper FJ, Vederas JC (eds) Biosynthesis—aromatic polyketides, isoprenoids, alkaloids. Springer, Berlin, pp 207–243

    Google Scholar 

  33. Ober D (2003) Chemical ecology of alkaloids exemplified with the pyrrolizidines. In: Romeo JTBT-RA in P (ed) Integrative phytochemistry: from ethnobotany to molecular ecology. Elsevier, Amsterdam, pp 203–230

    Chapter  Google Scholar 

  34. Schimming O, Challinor VL, Tobias NJ, Adihou H, Grun P, Poschel L, Richter C, Schwalbe H, Bode HB (2015) Structure, biosynthesis, and occurrence of bacterial pyrrolizidine alkaloids. Angew Chem (International ed in English) 54:12702–12705. https://doi.org/10.1002/anie.201504877

    Article  CAS  Google Scholar 

  35. Joosten L, van Veen JA (2011) Defensive properties of pyrrolizidine alkaloids against microorganisms. Phytochem Rev 10:127–136. https://doi.org/10.1007/s11101-010-9204-y

    Article  PubMed  CAS  Google Scholar 

  36. Ruan J, Liao C, Ye Y, Lin G (2014) Lack of metabolic activation and predominant formation of an excreted metabolite of nontoxic platynecine-type pyrrolizidine alkaloids. Chem Res Toxicol 27:7–16. https://doi.org/10.1021/tx4004159

    Article  PubMed  CAS  Google Scholar 

  37. Palma L, Muñoz D, Berry C, Murillo J, Caballero P (2014) Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins 6:3296–3325. https://doi.org/10.3390/toxins6123296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Schmidt R, Ulanova D, Wick LY, Bode HB, Garbeva P (2019) Microbe-driven chemical ecology: past, present and future. ISME J 13:2656–2663. https://doi.org/10.1038/s41396-019-0469-x

    Article  PubMed  Google Scholar 

  39. Vuong HQ, McFrederick QS (2019) Comparative genomics of wild bee and flower isolated lactobacillus reveals potential adaptation to the bee host. Genome Biol Evol 11:2151–2161. https://doi.org/10.1093/gbe/evz136

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Sun Z, Zhang W, Guo C, Yang X, Liu W, Wu Y, Song Y, Kwok LY, Cui Y, Menghe B, Yang R, Hu L, Zhang H (2015) Comparative genomic analysis of 45 type strains of the genus Bifidobacterium: a snapshot of its genetic diversity and evolution. PLoS ONE 10:e0117912–e0117912. https://doi.org/10.1371/journal.pone.0117912

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Ellegaard KM, Tamarit D, Javelind E, Olofsson TC, Andersson SGE, Vasquez A (2015) Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics 16:284. https://doi.org/10.1186/s12864-015-1476-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Gil MI, Ferreres F, Ortiz A, Subra E, Tomas-Barberan FA (1995) Plant phenolic metabolites and floral origin of rosemary honey. J Agric Food Chem 43:2833–2838. https://doi.org/10.1021/jf00059a012

    Article  CAS  Google Scholar 

  43. Ferreres F, García-Viguera C, Tomás-Lorente F, Tomás-Barberán FA (1993) Hesperetin: a marker of the floral origin of citrus honey. J Sci Food Agric 61:121–123. https://doi.org/10.1002/jsfa.2740610119

    Article  CAS  Google Scholar 

  44. Truchado P, Martos I, Bortolotti L, Sabatini AG, Ferreres F, Tomas-Barberan FA (2009) Use of quinoline alkaloids as markers of the floral origin of chestnut honey. J Agric Food Chem 57:5680–5686. https://doi.org/10.1021/jf900766v

    Article  PubMed  CAS  Google Scholar 

  45. Baracchi D, Brown MJF, Chittka L (2015) Behavioural evidence for self-medication in bumblebees? F1000Research 4:73. https://doi.org/10.12688/f1000research.6262.2

    Article  PubMed  PubMed Central  Google Scholar 

  46. Negri P, Villalobos E, Szawarski N, Damiani N, Gende L, Garrido M, Maggi M, Quintana S, Lamattina L, Eguaras M (2019) Towards precision nutrition: a novel concept linking phytochemicals, immune response and honey bee health. Insects. https://doi.org/10.3390/insects10110401

    Article  PubMed  PubMed Central  Google Scholar 

  47. 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. https://doi.org/10.1128/mBio.02164-15

    Article  PubMed  PubMed Central  Google Scholar 

  48. Price-Whelan A, Dietrich LEP, Newman DK (2006) Rethinking “secondary” metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78. https://doi.org/10.1038/nchembio764

    Article  PubMed  CAS  Google Scholar 

  49. Davies J, Ryan KS (2012) Introducing the parvome: bioactive compounds in the microbial world. ACS Chem Biol 7:252–259. https://doi.org/10.1021/cb200337h

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Rita Resca of Renolab srl and her staff for the analysis of bacterial metabolites. This study was performed within the frame of CREA research facilities by using institutional resources, and partially supported by EU Reg. 1308/2013 of the Italian Ministry of Agriculture 2016–2019.

Author information

Authors and Affiliations

  1. Council for Agricultural Research and Economics (CREA), Research Center for Agriculture and Environment, Via di Corticella 133, 40128, Bologna, Italy

    L. M. Manici, M. L. Saccà & M. Lodesani

  2. CREA-AA, via di Corticella 133, Bologna, Italy

    L. M. Manici

Authors
  1. L. M. Manici
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. L. Saccà
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Lodesani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MLM: investigation-secondary metabolites; data analysis; writing—original draft. SML: investigation and methodology-bacteria, writing—review & editing. LM: investigation-methodology-honey bees and Varroa.

Corresponding author

Correspondence to L. M. Manici.

Ethics declarations

Conflict of interest

The authors declare no potential conflict of interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manici, L.M., Saccà, M.L. & Lodesani, M. Secondary Metabolites Produced by Honey Bee-Associated Bacteria for Apiary Health: Potential Activity of Platynecine. Curr Microbiol 77, 3441–3449 (2020). https://doi.org/10.1007/s00284-020-02153-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-02153-6

Search

Navigation