Novel solid-state fermentation of bee-collected pollen emulating the natural fermentation process of bee bread

Food Microbiology

Volumn 82, Issue , 2019, Pages 218-230

  Di Cagno, Raffaella ^a   Filannino, Pasquale ^b   Cantatore, Vincenzo ^b   Gobbetti, Marco ^a  

^a FREE UNIVERSITY OF BOZEN BOLZANO   (Italy)

^b UNIVERSITY OF BARI   (Italy)

Author keywords

Bee bread; Bee collected pollen; Fermentation; Honeybee; Lactobacillus kunkeei

Indexed keywords

ANTIINFECTIVE AGENT; PROPOLIS;

ANIMAL; BEE; CHEMISTRY; CLASSIFICATION; FERMENTATION; FLOWER; FOOD CONTROL; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; HANSENIASPORA; ISOLATION AND PURIFICATION; IVY; LACTOBACILLALES; LACTOBACILLUS; METABOLISM; MICROBIOLOGY; MICROFLORA; ORGANISMAL INTERACTION; POLLEN; SPECIES DIFFERENCE;

ANIMALS; ANTI-INFECTIVE AGENTS; BEES; FERMENTATION; FLOWERS; FOOD MICROBIOLOGY; GASTROINTESTINAL TRACT; HANSENIASPORA; HEDERA; LACTOBACILLALES; LACTOBACILLUS; MICROBIAL INTERACTIONS; MICROBIOTA; POLLEN; PROPOLIS; SPECIES SPECIFICITY;

EID: 85062223616     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2019.02.007     Document Type: Article

References (76)

1. Denisow, B., Denisow–Pietrzyk, M., Biological and therapeutic properties of bee pollen: a review. J. Sci. Food Agric. 96 (2016), 4303–4309 https://doi.org/10.1002/jsfa.7729.
2. Akeson, W.R., Stahmann, M.A., A pepsin pancreatin digest index of protein quality evaluation. J. Nutr. 83 (1964), 257–261 https://doi.org/10.1093/jn/83.3.257.
3. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997), 3389–3402 https://doi.org/10.1093/nar/25.17.3389.
4. Anderson, K.E., Sheehan, T.H., Eckholm, B.J., Mott, B.M., DeGrandi–Hoffman, G., An emerging paradigm of colony health: microbial balance of the honey bee and hive (Apis mellifera). Insectes Soc. 58 (2011), 431–444 https://doi.org/10.1007/s00040-011-0194-6.
5. Anderson, K.E., Sheehan, T.H., Mott, B.M., Maes, P., Snyder, L., Schwan, M.R., Walton, A., Jones, B.M., Corby-Harris, V., Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One, 8, 2013, e83125 https://doi.org/10.1371/journal.pone.0083125.
6. Anderson, K.E., Carroll, M.J., Sheehan, T.I.M., Mott, B.M., Maes, P., Corby‐Harris, V., Hive‐stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol. Ecol. 23 (2014), 5904–5917 https://doi.org/10.1111/mec.12966.
7. Anđelković, B., Jevtić, G., Mladenović, M., Marković, J., Petrović, M., Nedić, N., Quality of pollen and honey bee bread collected in spring. J. Hyg. Eng. Des. 1 (2012), 275–277.
8. Asenjo, F., Olmos, A., Henriquez-Piskulich, P., Polanco, V., Aldea, P., Ugalde, J.A., Trombert, A.N., Genome sequencing and analysis of the first complete genome of Lactobacillus kunkeei strain MP2, an Apis mellifera gut isolate. PeerJ, 4, 2016 e1950 https://doi.org/10.7717/peerj.1950.
9. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976), 248–254 https://doi.org/10.1016/0003-2697(76)90527-3.
10. Brindza, J., Gróf, J., Bacigálová, K., Ferianc, P., Tóth, D., Pollen microbial colonization and food safety. Acta Chim. Slovaca 3 (2010), 95–102.
11. Campos, M.G., Bogdanov, S., de Almeida-Muradian, L.B., Szczesna, T., Mancebo, Y., Frigerio, C., Ferreira, F., Pollen composition and standardisation of analytical methods. J. Apicult. Res. 47 (2008), 154–161 https://doi.org/10.1080/00218839.2008.11101443.
12. Campos, M., Frigerio, C., Lopes, J., Bogdanov, S., What is the future of Bee-Pollen?. J. ApiProduct ApiMed. Sci. 2 (2010), 131–144 https://10.3896/IBRA.4.02.4.01.
13. Carroll, M.J., Brown, N., Goodall, C., Downs, A.M., Sheenan, T.H., Anderson, K.E., Honey bees preferentially consume freshly-stored pollen. PLoS One, 12, 2017, e0175933 https://doi.org/10.1371/journal.pone.0175933.
14. Celano, G., De Angelis, M., Minervini, F., Gobbetti, M., Different flour microbial communities drive to sourdoughs characterized by diverse bacterial strains and free amino acid profiles. Front. Microbiol., 7, 2016, 1770 https://doi.org/10.3389/fmicb.2016.01770.
15. Church, F.C., Swaisgood, H.E., Porter, D.H., Catignani, G.L., Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. J. Dairy Sci. 66 (1983), 1219–1227 https://doi.org/10.3168/jds.S0022-0302(83)81926-2.
16. Coda, R., Rizzello, C.G., Nigro, F., De Angelis, M., Arnault, P., Gobbetti, M., Long-term fungi inhibitory activity of water-soluble extract from Phaseolus vulgaris cv. Pinto and sourdough lactic acid bacteria during bread storage. Appl. Environ. Microbiol. 74 (2008), 7391–7398 https://doi.org/10.1128/AEM.01420-08.
17. Collin, S., Vanhavre, T., Bodart, E., Bouseta, A., Heat treatment of pollens: impact on their volatile flavor constituents. J. Agric. Food Chem. 43 (1995), 444–448 https://doi.org/10.1021/jf00050a035.
18. Cook, S., Awmack, C., Murray, D., Williams, I., Are honey bees' foraging preferences affected by pollen amino acid composition?. Ecol. Entomol. 28 (2003), 622–627 https://doi.org/10.1046/j.1365-2311.2003.00548.x.
19. Corby-Harris, V., Maes, P., Anderson, K.E., The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS One, 9, 2014, e95056 https://doi.org/10.1371/journal.pone.0095056.
20. De Angelis, M., Corsetti, A., Tosti, N., Rossi, J., Corbo, M.R., Gobbetti, M., Characterization of non-starter lactic acid bacteria from Italian ewe cheeses based on phenotypic, genotypic, and cell wall protein analyses. Appl. Environ. Microbiol. 67 (2001), 2011–2020 https://doi.org/10.1128/AEM.67.5.2011-2020.2001.
21. De Angelis, M., Siragusa, S., Berloco, M., Caputo, L., Settanni, L., Alfonsi, G., Amerio, M., Grandi, A., Ragni, A., Gobbetti, M., Selection of potential probiotic lactobacilli from pig feces to be used as additives in pelleted feeding. Res. Microbiol. 157 (2006), 792–801 https://doi.org/10.1016/j.resmic.2006.05.003.
22. De Grandi-Hoffman, G., Eckholm, B.J., Hua-Huang, M., A comparison of bee bread made by Africanized and European honey bees (Apis mellifera) and its effects on hemolymph protein titers. Apidologie 44 (2013), 52–63 https://doi.org/10.1007/s13592-012-0154-9.
23. De Melo, A.A.M., Estevinho, M.L.M.F., Almeida‐Muradian, L.B., A diagnosis of the microbiological quality of dehydrated bee‐pollen produced in Brazil. Lett. Appl. Microbiol. 61 (2015), 477–483 https://doi.org/10.1111/lam.12480.
24. Dias, L.G., Tolentino, G., Pascoal, A., Estevinho, L.M., Effect of processing conditions on the bioactive compounds and biological properties of bee pollen. J. Apicult. Res. 55 (2016), 357–365 https://doi.org/10.1080/00218839.2016.1248109.
25. Ellis, A., Hayes, G., An evaluation of fresh versus fermented diets for honey bees (Apis mellifera). J. Apicult. Res. 48 (2009), 215–216 https://doi.org/10.3896/IBRA.1.48.3.11.
26. Engel, P., Martinson, V.G., Moran, N.A., Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. U. S. A 109 (2012), 11002–11007 https://doi.org/10.1073/pnas.1202970109.
27. Filannino, P., Di Cagno, R., Addante, R., Pontonio, E., Gobbetti, M., Metabolism of fructophilic lactic acid bacteria isolated from Apis mellifera L. bee-gut: a focus on the phenolic acids as external electron acceptors. Appl. Environ. Microbiol. 82 (2016), 6899–6911 https://doi.org/10.1128/AEM.02194-16.
28. Gilliam, M., Microbiology of pollen and bee bread: the genus Bacillus. Apidologie 10 (1979), 269–274.
29. Gilliam, M., Microbiology of pollen and bee bread: The yeasts. Apidologie 10 (1979), 43–53.
30. Gilliam, M., Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol. Lett. 155 (1997), 1–10 https://doi.org/10.1111/j.1574-6968.1997.tb12678.x.
31. Gilliam, M., Prest, D.B., Lorenz, B.J., Microbiology of pollen and bee bread: taxonomy and enzymology of molds. Apidologie 20 (1989), 53–68.
32. Goebel, B.M., Stackebrandt, E., Cultural and phylogenetic analysis of mixed microbial populations found in natural and commercial bioleaching environments. Appl. Environ. Microbiol. 60 (1994), 1614–1621.
33. González, G., Hinojo, M.J., Mateo, R., Medina, A., Jiménez, M., Occurrence of mycotoxin producing fungi in bee pollen. Int. J. Food Microbiol. 105 (2005), 1–9 https://doi.org/10.1016/j.ijfoodmicro.2005.05.001.
34. Hani, B., Dalila, B., Saliha, D., Daoud, H., Mouloud, G., Seddik, K., Microbiological sanitary aspects of pollen. Adv. Environ. Biol. 6 (2012), 1415–1420.
35. Herbert, E.W., Shimanuki, H., Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie 9 (1978), 33–40.
36. Hesse, M., Halbritter, H., Zetter, R., Weber, M., Buchner, R., Frosch-Radivo, A., Ulrich, S., Pollen Terminology. An illustrated hand book. 2009, Springer, Wien.
37. Human, H., Nicolson, S.W., Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry 67 (2006), 1486–1492 https://doi.org/10.1016/j.phytochem.2006.05.023.
38. Kaplan, M., Karaoglu, Ö., Eroglu, N., Silici, S., Fatty acid and proximate composition of bee bread. Food Technol. Biotechnol. 54 (2016), 497–504 https://doi.org/10.17113/ftb.54.04.16.4635.
39. Kieliszek, M., Piwowarek, K., Kot, A.M., Błażejak, S., Chlebowska-Śmigiel, A., Wolska, I., Pollen and bee bread as new health-oriented products: A review. Trends Food Sci. Technol. 71 (2018), 170–180 https://doi.org/10.1016/j.tifs.2017.10.021.
40. Kostić, A.Ž., Petrović, T.S., Krnjaja, V.S., Nedić, N.M., Tešić, Ž.L., Milojković-Opsenica, D.M., Barać, M.B., Stanojevic, S.P., Pešić, M.B., Mold/aflatoxin contamination of honey bee collected pollen from different Serbian regions. J. Apicult. Res. 56 (2017), 13–20 https://doi.org/10.1080/00218839.2016.1259897.
41. Lee, F.J., Rusch, D.B., Stewart, F.J., Mattila, H.R., Newton, I.L., Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ. Microbiol. 17 (2015), 796–815 https://doi.org/10.1111/1462-2920.12526.
42. Linjordet, M.S., A comparative analysis of lactic acid bacteria isolated from honeybee gut and flowers, with focus on phylogeny and plasmid profiling. 2016, Norwegian University of Life Sciences, Oslo, Norway http://hdl.handle.net/11250/2398654.
43. Loncaric, I., Heigl, H., Licek, E., Moosbeckhofer, R., Busse, H.J., Rosengarten, R., Typing of Pantoea agglomerans isolated from colonies of honey bees (Apis mellifera) and culturability of selected strains from honey. Apidologie 40 (2009), 40–54 https://doi.org/10.1051/apido/2008062.
44. Loper, G.M., Standifer, L.N., Thompson, M.J., Gilliam, M., Biochemistry and microbiology of bee-collected almond (Prunus dulcis) pollen and bee bread. I-Fatty Acids, Sterols, Vitamins and Minerals. Apidologie 11 (1980), 63–73.
45. Markiewicz-Żukowska, R., Naliwajko, S.K., Bartosiuk, E., Moskwa, J., Isidorov, V., Soroczyńska, J., Borawska, M.H., Chemical composition and antioxidant activity of beebread, and its influence on the glioblastoma cell line (U87MG). J. Apicult. Sci. 57 (2013), 147–157 https://doi.org/10.2478/jas-2013-0025.
46. Maruyama, H., Sakamoto, T., Araki, Y., Hara, H., Anti-inflammatory effect of bee pollen ethanol extract from Cistus sp. of Spanish on carrageenan-induced rat hind paw edema. BMC Complement Altern. Med., 10, 2010, 30 https://doi.org/10.1186/1472-6882-10-30.
47. Masoud, W., Jespersen, L., Pectin degrading enzymes in yeasts involved in fermentation of Coffea arabica in East Africa. Int. J. Food Microbiol. 110 (2006), 291–296 https://doi.org/10.1016/j.ijfoodmicro.2006.04.030.
48. Mattila, H.R., Rios, D., Walker-Sperling, V.E., Roeselers, G., Newton, I.L., Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. PLoS One, 7, 2012, e32962 https://doi.org/10.1371/journal.pone.0032962.
49. Mauriello, G., De Prisco, A., Di Prisco, G., La Storia, A., Caprio, E., Microbial characterization of bee pollen from the Vesuvius area collected by using three different traps. PLoS One, 12, 2017, e0183208 https://doi.org/10.1371/journal.pone.0183208.
50. McFrederick, Q.S., Wcislo, W.T., Taylor, D.R., Ishak, H.D., Dowd, S.E., Mueller, U.G., Environment orkin: whence do bees obtain acidophilic bacteria?. Mol. Ecol. 21 (2012), 1754–1768 https://doi.org/10.1111/j.1365-294X.2012.05496.x.
51. Medina, Á., González, G., Sáez, J.M., Mateo, R., Jiménez, M., Bee pollen, a substrate that stimulates ochratoxin A production by Aspergillus ochraceus Wilh. Syst. Appl. Microbiol. 27 (2004), 261–267 https://doi.org/10.1078/072320204322881880.
52. Mutsaers, M., van Blitterswijk, H., van‘t Leven, L., Kerkvliet, J., van de Waerdt, J., Bee products properties, processing and marketing. 2005, Agromisa Foundation, Wageningen, The Netherlands.
53. Nagai, T., Nagashima, T., Myoda, T., Inoue, R., Preparation and functional properties of extracts from bee bread. Nahrung 48 (2004), 226–229 https://doi.org/10.1002/food.200300421.
54. Nardoni, S., D'Ascenzi, C., Rocchigiani, G., Moretti, V., Mancianti, F., Occurrence of moulds from bee pollen in Central Italy-A preliminary study. Ann. Agric. Environ. Med. 23 (2016), 103–105 https://doi.org/10.5604/12321966.1196862.
55. Podrižnik, B., Božič, J., Maturation and stratification of antibacterial activity and total phenolic content of bee bread in honey comb cells. J. Apicult. Res. 54 (2015), 81–92 https://doi.org/10.1080/00218839.2015.1090774.
56. Quiroga, E.N., Sampietro, A.R., Vattuone, M.A., Screening antifungal activities of selected medicinal plants. J. Ethnopharmacol. 74 (2001), 89–96 https://doi.org/10.1016/S0378-8741(00)00350-0.
57. Rangberg, A., Diep, D.B., Rudi, K., Amdam, G.V., Paratransgenesis: an approach to improve colony health and molecular insight in honey bees (Apis mellifera)?. Integr. Comp. Biol. 52 (2012), 89–99 https://doi.org/10.1093/icb/ics089.
58. Rizzello, C.G., Nionelli, L., Coda, R., De Angelis, M., Gobbetti, M., Effect of sourdough fermentation on stabilisation, and chemical and nutritional characteristics of wheat germ. Food Chem. 119 (2010), 1079–1089 https://doi.org/10.1016/j.foodchem.2009.08.016.
59. Salazar-González, C., Díaz-Moreno, C., The nutritional and bioactive aptitude of bee pollen for a solid-state fermentation process. J. Apicult. Res. 55 (2016), 161–175 https://doi.org/10.1080/00218839.2016.1205824.
60. Sanger, F., Nicklen, S., Coulson, A.R., DNA sequencing with chainterminating inhibitors. Proc. Natl. Acad. Sci. U. S. A 74 (1977), 5463–5467 https://doi.org/10.1073/pnas.74.12.5463.
61. Schillinger, U., Lücke, F.K., Antibacterial activity of Lactobacillus sake isolated from meat. Appl. Environ. Microbiol. 55 (1989), 1901–1906.
62. Singleton, V.L., Rossi, J.A., Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16 (1965), 144–158.
63. Siragusa, S., Di Cagno, R., Ercolini, D., Minervini, F., Gobbetti, M., De Angelis, M., Taxonomic structure and monitoring of the dominant population of lactic acid bacteria during wheat flour sourdough type I propagation using Lactobacillus sanfranciscensis starters. Appl. Environ. Microbiol. 75 (2009), 1099–1109 https://doi.org/10.1128/AEM.01524-08.
64. Soares de Arruda, V.A., Santos Pereira, A.A., Silva de Freitas, A., Barth, O.M., de Almeida-Muradian, L.B., Dried bee pollen: B complex vitamins, physicochemical and botanical composition. J. Food Compos. Anal. 29 (2013), 100–105 https://doi.org/10.1016/j.jfca.2012.11.004.
65. Sobral, F., Calhelha, R.C., Barros, L., Dueñas, M., Tomás, A., Santos-Buelga, C., Vilas-Boas, M., Ferreira, I.C., Flavonoid composition and antitumor activity of bee bread collected in northeast Portugal. Molecules, 22, 2017, 248 https://doi.org/10.3390/molecules22020248.
66. Tamarit, D., Ellegaard, K.M., Wikander, J., Olofsson, T., Vasquez, A., Andersson, S.G., Functionally structured genomes in Lactobacillus kunkeei colonizing the honey crop and food products of honeybees and stingless bees. Genome Biol. Evol. 7 (2015), 1455–1473 https://doi.org/10.1093/gbe/evv079.
67. Torriani, S., Felis, G.E., Dellaglio, F., Differentiation of Lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA gene sequence analysis and multiplex PCR assay with recA gene-derived primers. Appl. Environ. Microbiol. 67 (2001), 3450–3454 https://doi.org/10.1128/AEM.67.8.3450-3454.2001.
68. Urcan, A., Mărghitaş, L.A., Dezmirean, D.S., Bobiş, O., Bonta, V., Mureşan, C.I., Mărgăoan, R., Chemical composition and biological activities of beebread-review. Bull. Univ. Agric. Sci. Vet. Med. Cluj. Napoca 74 (2017), 6–14 https://doi.org/10.15835/buasvmcn-asb:12646.
69. Vanderplanck, M., Moerman, R., Rasmont, P., Lognay, G., Wathelet, B., Wattiez, R., Michez, D., How does pollen chemistry impact development and feeding behaviour of polylectic bees?. PLoS One, 9, 2014, e86209 https://doi.org/10.1371/journal.pone.0086209.
70. Vásquez, A., Olofsson, T.C., The lactic acid bacteria involved in the production of bee pollen and bee bread. J. Apicult. Res. 48 (2009), 189–195 https://doi.org/10.3896/IBRA.1.48.3.07.
71. Vásquez, A., Olofsson, T.C., Sammataro, D., A scientific note on the lactic acid bacterial flora in honeybees in the USA—a comparison with bees from Sweden. Apidologie 40 (2009), 26–28 https://doi.org/10.1051/apido:2008063.
72. Xiao, W., Yeast protocols. 2006, Humana Press, Totowa https://doi.org/10.1007/978-1-4939-0799-1.
73. Yang, K., Wu, D., Ye, X., Liu, D., Chen, J., Sun, P., Characterization of chemical composition of bee pollen in China. J. Agric. Food Chem. 61 (2013), 708–718 https://doi.org/10.1021/jf304056b.
74. Zhou, W., Yan, Y., Mi, J., Zhang, H., Lu, L., Luo, Q., Li, X., Zeng, X., Cao, Y., Simulated digestion and fermentation in vitro by human gut microbiota of polysaccharides from bee collected pollen of Chinese wolfberry. J. Agric. Food Chem. 66 (2018), 898–907 https://doi.org/10.1021/acs.jafc.7b05546.
75. Zuluaga, C.M., Serrato, J.C.B., Quicazán, M.C., Valorization alternatives of Colombian bee-pollen for its use as food resource – a structured review. Vitae 21 (2014), 237–247.
76. Zuluaga, C.M., Serrato, J.C.B., Quicazán, M.C., Chemical, nutritional and bioactive characterization of Colombian bee-bread. Chem. Eng. Trans. 43 (2015), 175–180, 10.3303/CET1543030.