In vitro Effects of Prebiotics and Synbiotics on Apis cerana Gut Microbiota

LV, MINGKUI; LEI, QINGZHI; YIN, HUAJUAN; HU, TIANNIAN; WANG, SIFAN; DONG, KUN; PAN, HONGBIN; LIU, YIQIU; LIN, QIUYE; CAO, ZHENHUI

doi:10.33073/pjm-2021-049

Abstract

This study aimed to investigate in vitro effects of the selected prebiotics alone, and in combination with two potential probiotic Lactobacillus strains on the microbial composition of Apis cerana gut microbiota and acid production. Four prebiotics, inulin, fructo-oligosaccharides, xylo-oligosaccharides, and isomalto-oligosaccharides were chosen, and glucose served as the carbon source. Supplementation of this four prebiotics increased numbers of Bifidobacterium and lactic acid bacteria while decreasing the pH value of in vitro fermentation broth inoculated with A. cerana gut microbiota compared to glucose. Then, two potential probiotics derived from A. cerana gut at different dosages, Lactobacillus helveticus KM7 and Limosilactobacillus reuteri LP4 were added with isomalto-oligosaccharides in fermentation broth inoculated with A. cerana gut microbiota, respectively. The most pronounced impact was observed with isomalto-oligosaccharides. Compared to isomalto-oligosaccharides alone, the combination of isomalto-oligosaccharides with both lactobacilli strains induced the growth of Bifidobacterium, LAB, and total bacteria and reduced the proliferation of Enterococcus and fungi. Consistent with these results, the altered metabolic activity was observed as lowered pH in in vitro culture of gut microbiota supplemented with isomalto-oligosaccharides and lactobacilli strains. The symbiotic impact varied with the types and concentration of Lactobacillus strains and fermentation time. The more effective ability was observed with IMO combined with L. helveticus KM7. These results suggested that isomalto-oligosaccharides could be a potential prebiotic and symbiotic with certain lactobacilli strains on A. cerana gut microbiota.

References

Abdel-Moneim AME, Elbaz AM, Khidr RES, Badri FB. Effect of in ovo inoculation of Bifidobacterium spp. on growth performance, thyroid activity, ileum histomorphometry, and microbial enumeration of broilers. Probiotics Antimicrob Proteins. 2020 Sep; 12(3):873–882. https://doi.org/10.1007/s12602-019-09613-x
Search in Google Scholar Back to article
Audisio MC, Sabaté DC, Benítez-Ahrendts MR. Effect of Lactobacillus johnsonii CRL1647 on different parameters of honeybee colonies and bacterial populations of the bee gut. Benef Microbes. 2015 Oct 15;6(5):687–695. https://doi.org/10.3920/BM2014.0155
Search in Google Scholar Back to article
Carlson J, Erickson J, Hess J, Gould T, Slavin J. Prebiotic dietary fiber and gut health: comparing the in vitro fermentations of beta-glucan, inulin and xylooligosaccharide. Nutrients. 2017 Dec 15; 9(12):1361. https://doi.org/10.3390/nu9121361
Search in Google Scholar Back to article
Chen C, Liu Z, Luo Y, Xu Z, Wang S, Zhang X, Dai R, Gao J, Chen X, Guo H, et al. Managed honeybee colony losses of the Eastern honeybee (Apis cerana) in China (2011–2014). Apidologie. 2017 Sep;48(5):692–702. https://doi.org/10.1007/s13592-017-0514-6
Search in Google Scholar Back to article
Dai P, Yan Z, Ma S, Yang Y, Wang Q, Hou C, Wu Y, Liu Y, Diao Q. The herbicide glyphosate negatively affects midgut bacterial communities and survival of honey bee during larvae reared in vitro. J Agric Food Chem. 2018 Jul 25;66(29):7786–7793. https://doi.org/10.1021/acs.jafc.8b02212
Search in Google Scholar Back to article
Driessen FM, Deboer R. Fermented milks with selected intestinal bacteria – a healthy trend in new products. Neth Milk Dairy J. 1989;43(3):367–382.
Search in Google Scholar Back to article
Duan X, Zhao B, Jin X, Cheng X, Huang S, Li J. Antibiotic treatment decrease the fitness of honeybee (Apis mellifera) larvae. Insects. 2021 Mar 30;12(4):301. https://doi.org/10.3390/insects12040301
Search in Google Scholar Back to article
Ellegaard KM, Tamarit D, Javelind E, Olofsson TC, Andersson SGE, Vásquez A. Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics. 2015 Dec;16(1):284. https://doi.org/10.1186/s12864-015-1476-6
Search in Google Scholar Back to article
Fehlbaum S, Prudence K, Kieboom J, Heerikhuisen M, van den Broek T, Schuren F, Steinert R, Raederstorff D. In vitro fermentation of selected prebiotics and their effects on the composition and activity of the adult gut microbiota. Int J Mol Sci. 2018 Oct 10;19(10):3097. https://doi.org/10.3390/ijms19103097
Search in Google Scholar Back to article
Fünfhaus A, Ebeling J, Genersch E. Bacterial pathogens of bees. Curr Opin Insect Sci. 2018 Apr;26:89–96. https://doi.org/10.1016/j.cois.2018.02.008
Search in Google Scholar Back to article
Ge Y, Jing Z, Diao Q, He JZ, Liu YJ. Host species and geography differentiate honeybee gut bacterial communities by changing the relative contribution of community assembly processes. MBio. 2021 Jun 29;12(3):e0075121. https://doi.org/10.1128/mBio.00751-21
Search in Google Scholar Back to article
Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017 Aug;14(8):491–502. https://doi.org/10.1038/nrgastro.2017.75
Search in Google Scholar Back to article
Gilliam M, Prest DB. Fungi isolated from the intestinal contents of foraging worker honey bees, Apis mellifera. J Invertebr Pathol. 1972 Jul;20(1):101–103. https://doi.org/10.1016/0022-2011(72)90087-0
Search in Google Scholar Back to article
Gmeiner M, Kneifel W, Kulbe KD, Wouters R, De Boever P, Nollet L, Verstraete W. Influence of a synbiotic mixture consisting of Lactobacillus acidophilus 74-2 and a fructooligosaccharide preparation on the microbial ecology sustained in a simulation of the human intestinal microbial ecosystem (SHIME reactor). Appl Microbiol Biotechnol. 2000 Feb 1;53(2):219–223. https://doi.org/10.1007/s002530050011
Search in Google Scholar Back to article
Goffin D, Delzenne N, Blecker C, Hanon E, Deroanne C, Paquot M. Will isomalto-oligosaccharides, a well-established functional food in Asia, break through the European and American market? The status of knowledge on these prebiotics. Crit Rev Food Sci Nutr. 2011 Apr 14;51(5):394–409. https://doi.org/10.1080/10408391003628955
Search in Google Scholar Back to article
Henrique-Bana FC, Wang X, Costa GN, Spinosa WA, Miglioranza LHS, Scorletti E, Calder PC, Byrne CD, Gibson GR. In vitro effects of Bifidobacterium lactis-based synbiotics on human faecal bacteria. Food Res Int. 2020 Feb;128(Feb):108776. https://doi.org/10.1016/j.foodres.2019.108776
Search in Google Scholar Back to article
Houdelet C, Sinpoo C, Chantaphanwattana T, Voisin SN, Bocquet M, Chantawannakul P, Bulet P. Proteomics of anatomical sections of the gut of Nosema-infected Western Honeybee (Apis mellifera) reveals different early responses to Nosema spp. isolates. J Proteome Res. 2021 Jan 01;20(1):804–817. https://doi.org/10.1021/acs.jproteome.0c00658
Search in Google Scholar Back to article
Khalifa SAM, Elshafiey EH, Shetaia AA, El-Wahed AAA, Algethami AF, Musharraf SG, AlAjmi MF, Zhao C, Masry SHD, Abdel-Daim MM, et al. Overview of bee pollination and its economic value for crop production. Insects. 2021 Jul 31;12(8):688. https://doi.org/10.3390/insects12080688
Search in Google Scholar Back to article
Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T. Importance of pollinators in changing landscapes for world crops. Proc Biol Sci. 2007 Feb 07; 274(1608):303–313. https://doi.org/10.1098/rspb.2006.3721
Search in Google Scholar Back to article
Koleva P, Ketabi A, Valcheva R, Gänzle MG, Dieleman LA. Chemically defined diet alters the protective properties of fructo-oligosaccharides and isomalto-oligosaccharides in HLA-B27 transgenic rats. PLoS One. 2014 Nov 4;9(11):e111717. https://doi.org/10.1371/journal.pone.0111717
Search in Google Scholar Back to article
Kwong WK, Moran NA. Gut microbial communities of social bees. Nat Rev Microbiol. 2016 Jun;14(6):374–384. https://doi.org/10.1038/nrmicro.2016.43
Search in Google Scholar Back to article
Lei Q, Wang S, Yin H, Cheng Y, Yu H, Pan H, Lin Q, Cao Z. [Effects of Lactobacillus reuteri LP4 on the survival rate, intestinal microbiota composition and gut antimicrobial peptide gene expression in adult workers of Apis cerana Fabricius] (in Chinese). J Yunnan Agric Univ (Nat Sci). 2020;35(05):796–803.
Search in Google Scholar Back to article
Likotrafiti E, Tuohy KM, Gibson GR, Rastall RA. An in vitro study of the effect of probiotics, prebiotics and synbiotics on the elderly faecal microbiota. Anaerobe. 2014 Jun;27:50–55. https://doi.org/10.1016/j.anaerobe.2014.03.009
Search in Google Scholar Back to article
Logtenberg MJ, Akkerman R, Hobé RG, Donners KMH, Van Leeuwen SS, Hermes GDA, Haan BJ, Faas MM, Buwalda PL, Zoetendal EG, et al. Structure-specific fermentation of galacto-oligosaccharides, isomalto-oligosaccharides and isomalto/malto-polysaccharides by infant fecal microbiota and impact on dendritic cell cytokine responses. Mol Nutr Food Res. 2021 Aug;65(16):2001077. https://doi.org/10.1002/mnfr.202001077
Search in Google Scholar Back to article
Molly K, De Smet I, Nollet L, Vande Woestyne M, Verstraete W. Effect of lactobacilli on the ecology of the gastro-intestinal microbiota cultured in the SHIME reactor. Microb Ecol Health Dis. 1996 Mar;9(2):79–89. https://doi.org/10.3109/08910609609166446
Search in Google Scholar Back to article
Nainu F, Masyita A, Bahar MA, Raihan M, Prova SR, Mitra S, Emran TB, Simal-Gandara J. Pharmaceutical prospects of bee products: special focus on anticancer, antibacterial, antiviral, and antiparasitic properties. Antibiotics (Basel). 2021 Jul 06;10(7):822. https://doi.org/10.3390/antibiotics10070822
Search in Google Scholar Back to article
Okazaki Y, Katayama T. Consumption of non-digestible oligosaccharides elevates colonic alkaline phosphatase activity by up-regulating the expression of IAP-I, with increased mucins and microbial fermentation in rats fed a high-fat diet. Br J Nutr. 2019 Jan 28;121(2):146–154. https://doi.org/10.1017/S0007114518003082
Search in Google Scholar Back to article
Ortiz-Alvarado Y, Clark DR, Vega-Melendez CJ, Flores-Cruz Z, Domingez-Bello MG, Giray T. Antibiotics in hives and their effects on honey bee physiology and behavioral development. Biol Open. 2020 Jan 01;9(11):bio.053884. https://doi.org/10.1242/bio.053884
Search in Google Scholar Back to article
Pachla A, Ptaszyńska AA, Wicha M, Kunat M, Wydrych J, Oleńska E, Małek W. Insight into probiotic properties of lactic acid bacterial endosymbionts of Apis mellifera L. derived from the Polish apiary. Saudi J Biol Sci. 2021 Mar;28(3):1890–1899. https://doi.org/10.1016/j.sjbs.2020.12.040
Search in Google Scholar Back to article
Pandey KR, Naik SR, Vakil BV. Probiotics, prebiotics and synbiotics – a review. J Food Sci Technol. 2015 Dec;52(12):7577–7587. https://doi.org/10.1007/s13197-015-1921-1
Search in Google Scholar Back to article
Poeker SA, Geirnaert A, Berchtold L, Greppi A, Krych L, Steinert RE, de Wouters T, Lacroix C. Understanding the prebiotic potential of different dietary fibers using an in vitro continuous adult fermentation model (PolyFermS). Sci Rep. 2018 Dec;8(1):4318. https://doi.org/10.1038/s41598-018-22438-y
Search in Google Scholar Back to article
Ptaszyńska AA, Paleolog J, Borsuk G. Nosema ceranae infection promotes proliferation of yeasts in honey bee intestines. PLoS One. 2016 Oct 13;11(10):e0164477. https://doi.org/10.1371/journal.pone.0164477
Search in Google Scholar Back to article
Ramos OY, Basualdo M, Libonatti C, Vega MF. Current status and application of lactic acid bacteria in animal production systems with a focus on bacteria from honey bee colonies. J Appl Microbiol. 2020 May;128(5):1248–1260. https://doi.org/10.1111/jam.14469
Search in Google Scholar Back to article
Rastall RA, Gibson GR. Recent developments in prebiotics to selectively impact beneficial microbes and promote intestinal health. Curr Opin Biotechnol. 2015 Apr;32:42–46. https://doi.org/10.1016/j.copbio.2014.11.002
Search in Google Scholar Back to article
Raymann K, Bobay LM, Moran NA. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Mol Ecol. 2018 Apr;27(8):2057–2066. https://doi.org/10.1111/mec.14434
Search in Google Scholar Back to article
Raymann K, Shaffer Z, Moran NA. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol. 2017 Mar 14;15(3):e2001861. https://doi.org/10.1371/journal.pbio.2001861
Search in Google Scholar Back to article
Rycroft CE, Jones MR, Gibson GR, Rastall RA. A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. J Appl Microbiol. 2001 Nov 23;91(5):878–887. https://doi.org/10.1046/j.1365-2672.2001.01446.x
Search in Google Scholar Back to article
Sanders ME, Merenstein DJ, Reid G, Gibson GR, Rastall RA. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat Rev Gastroenterol Hepatol. 2019 Oct;16(10):605–616. https://doi.org/10.1038/s41575-019-0173-3
Search in Google Scholar Back to article
Śliżewska K, Chlebicz A. Synbiotics impact on dominant faecal microbiota and short-chain fatty acids production in sows. FEMS Microbiol Lett. 2019 Jul;366(13): fnz157. https://doi.org/10.1093/femsle/fnz157
Search in Google Scholar Back to article
Sorndech W, Nakorn KN, Tongta S, Blennow A. Isomalto-oligosaccharides: recent insights in production technology and their use for food and medical applications. LWT Food Sci Technol. 2018 Sep; 95:135–142. https://doi.org/10.1016/j.lwt.2018.04.098
Search in Google Scholar Back to article
Swanson KS, Gibson GR, Hutkins R, Reimer RA, Reid G, Verbeke K, Scott KP, Holscher HD, Azad MB, Delzenne NM, et al. The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics. Nat Rev Gastroenterol Hepatol. 2020 Nov;17(11):687–701. https://doi.org/10.1038/s41575-020-0344-2
Search in Google Scholar Back to article
Tandon D, Haque MM, Gote M, Jain M, Bhaduri A, Dubey AK, Mande SS. A prospective randomized, double-blind, placebo-controlled, dose-response relationship study to investigate efficacy of fructo-oligosaccharides (FOS) on human gut microflora. Sci Rep. 2019 Dec;9(1):5473. https://doi.org/10.1038/s41598-019-41837-3
Search in Google Scholar Back to article
Tornero-Martínez A, Cruz-Ortiz R, Jaramillo-Flores ME, Osorio-Díaz P, Ávila-Reyes SV, Alvarado-Jasso GM, Mora-Escobedo R. In vitro fermentation of polysaccharides from Aloe vera and the evaluation of antioxidant activity and production of short chain fatty acids. Molecules. 2019 Oct 07;24(19):3605. https://doi.org/10.3390/molecules24193605
Search in Google Scholar Back to article
Wang L, Hu L, Yan S, Jiang T, Fang S, Wang G, Zhao J, Zhang H, Chen W. Effects of different oligosaccharides at various dosages on the composition of gut microbiota and short-chain fatty acids in mice with constipation. Food Funct. 2017;8(5):1966–1978. https://doi.org/10.1039/C7FO00031F
Search in Google Scholar Back to article
Wang S, Gao J, Liu J, Zhao D. Morphometric characterization of Apis cerana hainana (Hymenoptera: Apidae) in Hainan province, P.R. China. J Apic Res. 2021 Mar 15;60(2):337–340. https://doi.org/10.1080/00218839.2020.1753326
Search in Google Scholar Back to article
Wang S. [Diversity of intestinal microbial and prebiotic function of lactic acid bacteria in Apis Cerana Fabricius] [Master Thesis] (in Chinese). Kunming (People’s Republic of China): Yunnan Agricultural University; 2018.
Search in Google Scholar Back to article
Watson D, O’Connell Motherway M, Schoterman MHC, van Neerven RJJ, Nauta A, van Sinderen D. Selective carbohydrate utilization by lactobacilli and bifidobacteria. J Appl Microbiol. 2013 Apr;114(4):1132–1146. https://doi.org/10.1111/jam.12105
Search in Google Scholar Back to article
Williams NT. Probiotics. Am J Health Syst Pharm. 2010 Mar 15; 67(6):449–458. https://doi.org/10.2146/ajhp090168
Search in Google Scholar Back to article

In vitro Effects of Prebiotics and Synbiotics on Apis cerana Gut Microbiota

Abstract

Paradigm

My account