BAL ARILARINDA GASTROİNTESTİNAL BAKTERİYEL FLORA

Bal arılarının (Apis mellifera) gastrointestinal sisteminde, mikroflora veya mikrobiyota olarak adlandırılan, çeşitli mikrobiyal tehditlere karşı korunmada, bazı metabolik faaliyetlerinde ve arı mahsullerinin üretiminde rol oynayan, arı bağışıklık sisteminde güçlü etki mekanizmalarına sahip, özgün bir mikroorganizma koleksiyonu bulunur. Özellikle yetişkin bal arıları çok zengin bir mikrofloraya sahiptirler. Arı sağlığının korunmasında en önemli ve dikkat çekici faktör, sahip oldukları bu mikrofloradır.Bal arıları (Apis mellifera) insanlar gibi toplu halde yaşar ve kovanda yaşamın devamlılığını sağlamak için iş birliği içinde çalışır. Üretken kolonilerde mikrobiyotadaki çeşitlilik artışı, arının gelişimsel yaşından beslenmesine, kovanın bulunduğu coğrafi konumdan iklim değişikliğine kadar çeşitli faktörlere bağlıdır. Bu bakteriyel topluluk kompozisyonundaki çeşitlilik azlığının da arının mevcut üretkenliğini olumsuz yönde etkileyebileceği belirtilmektedir. Bu derleme, arı yaşamı için büyük önem arz eden bağırsak temel mikroflorasının çeşitliliğini, edinim yollarını, arının gastrointestinal sistemindeki özel kolonizasyonunu ve bal arısı için fayda mekanizmalarını açıklamaktadır.

GASTROINTESTINAL BACTERIAL FLORA IN HONEY BEES

In the gastrointestinal tract of honey bees (Apis mellifera), there is a unique collection of microorganisms, called microflora or microbiota, which have various mgeyietabolic activities in the bee crops, which can protect against various microbial threats, and is linked to powerful mechanisms of action in the bee immune system. The adult honey bees especially have a rich microflora. Their microbiome is considered to be one of the most important and remarkable factors in maintaining bee health.Like humans, honey bees (Apis mellifera) are social creatures and work cooperatively to ensure the continuity of life in the hive. In productive colonies, the increasing diversity of microbiota depends on various factors, from the developmental age of the bee to its feeding, from the geographical location of the hive to the local climate. The lack of diversity of the bacterial community may negatively affect the productivity of the bee hive. This review describes the diversity of the honey bee intestinal core microflora, which are of great importance for bee life, the ways in which they acquire the bacteria, how they colonize in the gastrointestinal tract of bee and their associated beneficial mechanisms for honey bee survival.

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  • Ahn, JH, Hong, IP, Bok, J, Kim, BY, Song, J, Weon, HY 2012. Pyrosequencing analysis of the bacterial communities in the guts of honeybees Apis cerana and Apis mellifera in Korea. Journal of Microbiology, 50, s., 735–745. [PubMed: 23124740]
  • Alberoni, D, Gaggia, F, Baffoni, L, Gioia, DD 2016. Beneficial microorganisms for honeybees: Problems and progresses. Applied Microbiology and Biotechnology, 100, 22. DOI: 10.1007/s00253-016-7870–4.
  • Anderson, KE, Carroll, MJ, Sheehan, T, Mott, BM, Maes, P, Corby-Harris, V 2014. Hivestored pollen of honeybees: Many lines of evidence are consistent with pollen preservation, not nutrient conversion. Molecular Ecology, 23, 5904–5917. [PubMed: 25319366].
  • Anderson, KE, Sheehan, T, Eckholm, B, Mott, B, DeGrandi-Hoffman, G 2011. An emerging paradigm of colony health: Microbial balance of the honeybee and hive (Apis mellifera). Insectes Sociaux, 58, 431–444. doi: 10.1007/s00040- 011-0194-6
  • Anderson, KE, Sheehan, TH, Mott, BM, Maes, P, Snyder, L, Schwan, MR, Walton, A, Jones, BM, Corby-Harris, V 2013. Microbial ecology of the hive and pollination landscape: Bacterial associates from floral nectar, the alimentary tract and stored food of honeybees (Apis mellifera). PLoS ONE, 8e83125. [PubMed: 24358254]
  • Anjum, SI, Shah, AH, Aurongzeb, M, Kori, J, Azim MK, Ansari, MJ, Bin, L 2017. Characterization of gut bacterial flora of Apis mellifera from North-West Pakistan. Saudi Journal of Biological Sciences, 25, 388–392. DOI: 10.1016/j.sjbs.2017.05.008.
  • Babendreier, D, Joller, D, Romeis, J, Bigler, F, Widmer, F 2007. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol, 59(3), 600–10. DOI: 10.1111/j.1574-6941.2006.00249.x.
  • Bendel, JL 2002. Characterization of the normal flora of honeybee hives in Central Wisconsin. University of Winconsin-La Crosse, Journal of Undergraduate Research, Volume V (2002), Biology and Microbiology, 437–441. (URL: https://www.uwlax.edu/urc/jur-online/2002/)
  • Blatt, J, Roces, F 2002. The control of the proventriculus in the honeybee (Apis mellifera carnica L.) I. A dynamic process influenced by food quality and quantity?. Journal of Insect Physiology, 48(6), 643–654. DOI: 10.1016/s0022-1910(02)00090-2.
  • Bonilla-Rosso, G, Engel, P 2018. Functional roles and metabolic niches in the honeybee gut microbiota. Current Opinion in Microbiology, 43, 69–76. DOI: 10.1016/j.mib.2017.12.009.
  • Butler, È, Alsterfjord, M, Olofsson, TC, Karlsson, C, Malmström, J, Vásquez, A 2013. Proteins of novel lactic acid bacteria from Apis mellifera mellifera: An insight into the production of known extra-cellular proteins during microbial stress. BMC Microbiology,13, 235.
  • Corby-Harris, V, Maes, P, Anderson, KE 2014. The bacterial communities associated with honeybee (Apis mellifera) foragers. PLOS ONE, 9(4), e95056.
  • Crailsheim, K 1988. Regulation of food passage in the intestine of the honeybee (Apis mellifera L.). Journal of Insect Physiology, 34(2), 85–90. DOI:10.1016/0022-1910(88)90158-8.
  • 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. Microbial Biotechnology, 5(3), 307–17. DOI:10.1111/j.1751-7915.2011.00312.x.
  • Davis, FC 2004. Inside and outside influences. In: David FC (editor), The Honey Bee Inside Out, Bee Craft Limited, Warwickshire, s., 145–157.
  • Dong, Z-Xiang, Li, H-Yuan, Chen, Y-Fei, Wang, F., Deng, X-Yu, Lin, L-Bing, Zhang, Q-Lin, Li, J-Lian, Guo, J. 2020. Colonization Of The Gut Microbiota Of Honey Bee (Apis mellifera) Workers At Different Developmental Stages. Microbiological Research, 321, 1–12. DOI: 10.1016/j.micres.2019.126370
  • Endo, A, Salminen, S 2013. Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Systematic and Applied Microbiology, 36, 444–448. [PubMed: 23845309]
  • Engel, P, Bartlett, KD, Moran, NA 2015. The bacterium Frischella perrara causes scab formation in the gut of its honeybee host. Article in mBio, 6, 3. DOI: 10.1128/mBio.00193-15.
  • Engel, P, Martinson, VG, Moran, NA 2012. Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences U.S.A., 109, 11002–11007.
  • Evans, J, Lopez, D 2004. Bacterial probiotics induce an immune response in the honeybee (Hymenoptera: Apidae). Journal of Economic Entomology, 97, 752–756.
  • Forsgren, E, Olofsson, T, Vásquez, A, Fries, I 2010. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honeybee larvae. Apidologie, 41, 99–108.
  • Gilliam, M 1971. Microbial sterility of the intestinal content of the immature honeybee, Apis mellifera. Annals of the Entomological Society of America, 64(1), 315–316. DOI: 10.1093/aesa/64.1.315.
  • Gilliam, M 1997. Identification and roles of non-pathogenic microflora associated with honeybees. FEMS Microbiology Letters, 155, 1–10. DOI: 10.1111/j.1574-6968.1997.tb12678.x.
  • Gilliam, M, Morton, LH 1978. Bacteria belonging to the genus Bacillus isolated from honeybees, Apis mellifera. Fed 2,4-D and antibiotics (1). Apidologie, Springer Verlag, 9(3), pp.213–222.
  • Gilliam, M, Prest, DB 1972. Fungi isolated from the intestinal contents of foraging worker honeybees, Apis mellifera. Journal of Invertebrate Pathology, 20(1), 101–103. DOI: 10.1016/0022-2011(72)90087-0.
  • Gilliam, M, Prest, DB, Morton, HL 1974. Fungi isolated from honeybees, Apis mellifera. Fed 2,4-D and Antibiotics. Journal of Invertebrate Pathology, 24(2), 213–217. DOI: 10.1016/0022-2011(74)90013-5.
  • Gilliam, M, Valentine, DK 1976. Bacteria isolated from the intestinal contents of foraging worker honeybees, Apis mellifera: The genus Bacillus. Journal of Invertebrate Pathology, 28(2), 275–276. DOI:10.1016/0022-2011(76)90137-3.
  • Hall, AB, Tolonen, AC, Xavier, RJ 2017. Human genetic variation and the gut microbiome in disease. Nature Reviews Genetics, 18(11), 690–699. DOI: 10.1038/nrg.2017.63.
  • Hroncova, Z, Havlik, J, Killer, J, Doskocil, I, Tyl, J, Kamler, M, Titera, D, Hakl, J, Bunesova, V, Rada, V 2015. Variation in honey bee gut microbial diversity affected by ontogenetic stage, age and geographic location. PLoS ONE, 10, e0118707. DOI: 10.1371/journal.pone.0118707.
  • Janashia, I, Choiset, Y, Jozefiak, D, Déniel, F, Coton, E, Moosavi-Movahedi, AA, Haertlé, T 2018. Beneficial protective role of endogenous lactic acid bacteria against mycotic contamination of honeybee beebread. Probiotics and Antimicrobial Proteins, 10, 638–646. DOI: 10.1007/s12602-017-9379-2.
  • Jeyaprakash, A, Hoy, MA, Allsopp, MH 2003. Bacterial Diversity In Worker Adults Of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) Assessed Using 16S rRNA Sequences. Journal of Invertebrate Pathology, 84(2), 96–103. DOI: 10.1016/j.jip.2003.08.007.
  • Jones, JC, Myerscough, MR, Graham, S 2004. Honeybee nest thermoregulation: Diversity promotes stability. Science, 16, 402–404.
  • Kešnerová, L, Mars, RAT, Ellegaard, KM, Troilo, M, Sauer, U, Engel, P 2017. Disentangling Metabolic Functions Of Bacteria In The Honey Bee Gut. PLOS Biology, 15(12), e2003467. DOI:10.1371/journal.pbio.2003467.
  • Killer, J, Dubna,´ S, Sedlacek, I, Svec P 2014. 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. International Journal of Systematic and Evolutionary Microbiology, 64, 152–157. DOI: 10.1099/ijs.0.053033-0.
  • Killer, J, Kopec, J, Mrazek, J, Rada, V, Dubna, S, Marounek, M 2010. Bifidobacteria in the digestive tract of bumblebees. Anaerobe, 16, (2), 165–170. DOI: 10.1016/j.anaerobe.2009.07.007.
  • Koch, H, Schmid-Hempel, P 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences U.S.A.,108, 19288–19292.
  • Kwong WK, Mancenido, AL, Moran, NA 2017. Immune system stimulation by the native gut microbiota of honeybees. Royal Society Open Science, 4, 170003. DOI: 10.1098/rsos.170003.
  • Kwong, WK., Moran, NA 2016. Gut microbial communities of social bees. Nature reviews microbiology, 14, 374–84. DOI:10.1038/nrmicro.2016.43.
  • Kwong, WK, Engel, P, Koch, H, Moran, NA 2014. Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceedings of the National Academy of Sciences of the United States of America, 111, 11509–11514. [PubMed: 25053814]
  • 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. International Journal Of Systematic And Evolutionary Microbiology, 63, 2008–2018. DOI: 10.1099/ijs.0.044875-0.
  • Lamei, S 2018. The Effect of Honeybee-Specific Lactic Acid Bacteria on American Foulbrood Disease of Honeybees. Doktora Tezi. Swedish University of Agricultural Sciences and Lund University, Uppsala, Lund, İsveç, 59 s, 14–21. Lee, CY, Kime, RW 1984. The use of honey for clarifying apple juice. Journal of Apicultural Research & Bee World, 23, 45–49.
  • Lee, FJ, Rusch, DB, Stewart, FJ, Mattila, HR, Newton, ILG 2014. Saccharide breakdown and fermentation by the honeybee gut microbiome. Environmental Microbiology, 17(3), 796–815. DOI: 10.1111/1462-2920.12526.
  • Linjordet, SM 2016. A Comparative Analysis of Lactic Acid Bacteria Isolated from Honeybee Gut and Flowers, With Focus on Phylogeny and Plasmid Profile. Master Tezi. Norwegian University of Life Sciences, Department of Chemistry, Biotechnology and Food Science, Norveç, 37 s, 1-3, 18–20.
  • Ludvigsen, J 2013. Seasonal Trends In The Midgut Microbiota Of Honeybees. Yüksek Lisans Tezi. Norwegian University of Life Sciences, Department of Chemistry, Biotechnology and Food Science, 89 s, 9–15.
  • Ludvigsen, J, Rangberg, A, Avershina, E, Sekelja, M, Kreibich, C, Amdam, G, Rudi, K 2015. Shifts in the midgut/pyloric microbiota composition within a honeybee apiary throughout a season. Microbes and Environments, 30, 235–244.
  • 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. Molecular Ecology, 20,3, s., 619–628. DOI:10.1111/J.1365-294x.2010.04959.X.
  • Martinson, VG, Moy, J, Moran, N 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology, 78, 2830–2840. [PubMed: 22307297]
  • Mathialagan, M, Johnson, Edward, YSJT, David, PMM, Senthilkumar, M, Srinivasan, MR, Mohankumar, S 2018. Isolation, characterization and identification of probiotic lactic acid bacteria (LAB) from honey bees. International Journal of Current Microbiology and Applied Science, 7, 894–906. DOI: 10.20546/ijcmas.2018.704.096.
  • Mattila, HR, Rios, D, Walker-Sperling, VE, Roeselers, G, Newton, ILG 2012. Characterization of the active microbiotas associated with honeybees reveals healthier and broader communities when colonies are genetically diverse. PloS One, 7, e32962. DOI: 10.1371/journal.pone.0032962.
  • Mohr, KI, Tebbe, CC 2006. Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environmental Microbiology, 8, s., 258–272. PMID: 16423014
  • Moran, NA 2015. Genomics of the honeybee microbiome. Current Opinion in Insect Science, 10, 22–28. DOI: 10.1016/j.cois.2015.04.003.
  • 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. [PubMed: 22558460]
  • Mrazek, J, Strosova, L, Fliegerova, K, Kott, T, Kopecny, J 2008. Diversity of insect intestinal microflora. Folia Microbiologica (Praha), 53, 229–233. DOI: 10.1007/s12223-008-0032-z.
  • Olofsson, TC, Vásquez, A 2008. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Current Microbiology, 57, 356–363. [PubMed: 18663527]
  • Porrini, C, Mutinelli, F, Bortolotti, L, Granato, A, Laurenson, L, Roberts, K, Gallina, A, Silvester, N, Medrzycki, P, Renzi, T, Sgolastra, F, Lodesani, M 2016. The status of honey bee health in Italy: Results from the Nationwide Bee Monitoring Network. PLoS ONE11(5):e0155411.doi:10.1371/journal.pone.0155411.
  • Powell, JE, Martinson, VG, Urban-Mead, K, Moran, NA 2014. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Applied and Environmental Microbiology, 80, 7378–7387.
  • Rada, V, Machova, M, Huk, J, Marounek, M, Duskova, D 1997. Microflora in the honeybee digestive tract: Counts, characteristics and sensitivity to veterinary drugs. Apidologie, 28, 357–365.
  • Raghavan, KT, Jacob, AA, Chandran, H 2013. Honeybee gut flora as a source of LAB (Lactic Acid Bacteria) with probiotic capabilities. The Journal of Food Technology, 105, 126-134.
  • Rangberg, A, Diep, DB, Rudi, K, Amdam, GV 2012. Paratransgenesis: An approach to improve colony health and molecular insight in honey bees (Apis mellifera). Integrative and Comparative Biology, 52(1), 89–99. doi:10.1093/icb/ics089.
  • Raymann, K, Moran, AN 2018. The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion In Insect Science, 26, 97–104. DOI: 10.1016/j.cois.2018.02.012
  • Raymann, K, Shaffer, Z, Moran, NA 2017. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biology, 15, e2001861.
  • Rokop, ZP, Horton, MA, Newton, ILG 2015. Interactions between cooccurring lactic acid bacteria in honey bee hives. Applied and Environmental Microbiology, 81, 7261–7270. DOI:10.1128/AEM.01259-15.
  • Sabree, ZL, Hansen, AK, Moran, NA 2012. Independent studies using deep sequencing resolve the same set of core bacterial species dominating gut communities of honeybees. PLoS ONE, 7, e41250. [PubMed: 22829932]
  • Sammataro, D, Yoder, AJ 2012. Honey bee colony health: Challenges and sustainable solutions. CRC Press Taylor and Francis Group, LLC, International Standard Book Number- 13: 978-1-4398-7941-2, Ozkirim, A., s.,13–14.
  • Snowdon, JA, Cliver, DO 1996. Microorganisms in honey. International Journal of Food Microbiology, 31(1-3), 1–26. DOI:10.1016/0168-1605(96)00970-1
  • Tajabadi, N, Mardan, M, Manap, MYA., Shuhaimi, M, Meimandipour, A, Nateghi, L 2011. Detection and identification of Lactobacillus Bacteria found in the honey stomach of the giant honeybee Apis dorsata. Apidologie, Springer Verlag, 42 (5), 642–649. DOI: 10.1007/s13592-011-0069-x
  • URL-1, 2020. https://bee-health.extension.org/abdomen-of-the-honey-bee/ (18 Şubat 2020)
  • URL-2, 2020. https://infovisual.info/en/biology-animal/internal-anatomy-of-a-bee (18 Şubat 2020)
  • URL-3, 2020. https://www.uaex.edu/farm-ranch/special-programs/beekeeping/about-honey-bees.aspx/ (18 Şubat 2020).
  • URL-4, 2020. https://dickinsoncountyconservationboard.com/2017/05/17/see-the-larva-inside-the-indoor-bee-hive/ (18 Şubat 2020).
  • URL-5, 2020. https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi (18 Şubat 2020)
  • Vasquez, 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(3), [e33188]. DOI: 10.1371/journal.pone.0033188.
  • Vojvodic, S, Rehan, SM, Anderson, KE 2013. Microbial gut diversity of Africanized and European honeybee larval instars. PLoS ONE, 8:e72106. [PubMed: 23991051]
  • 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. Journal of Invertebrate Pathology, 102: 91–96. DOI: 10.1016/j.jip.2009.07.005.
  • Yun, JH, Jung, MJ, Kim, PS, Bae, JW 2018. Social status shapes the bacterial and fungal gut communities of the honeybee. Scientific Reports, 8 (1). DOI: 10.1038/s41598-018-19860-7.
  • Zheng, H, Powell, JE, Steele, MI, Dietrich, C, Moran, NA 2017. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings of the National Academy of Sciences U.S.A., 114:4775–4780.
Uludağ Arıcılık Dergisi-Cover
  • Başlangıç: 2001
  • Yayıncı: U.Ü.Arıcılık Geliştirme-Uygulama ve Araştırma Merkezi