Yeast Diversity in Honey Produced by Wild Honeybees at Different Elevations
Main Article Content
Abstract
Yeasts inhabit diverse natural environments, including the honeycombs of wild honeybee colonies residing at different elevations. This study investigates yeast populations in honeycombs located at two sampling sites, Bligo and Sukomulyo, Central Java Province, Indonesia, situated in a montane region at elevations of 131.1 and 676 meters above sea level, respectively. Out of the 40 yeast isolates collected, 12 distinct fingerprints were identified, representing ten strains across four species. Debaryomyces hansenii emerged as the predominant species, accounting for seven of the total strains, and being found at both sampling sites. The remaining species included Priceomyces melissophilus, Cystobasidium minutum, and Meyerozyma guillermondii. Overall, yeast abundance in this study was relatively low. The index of abundances (H') was higher in Bligo (0.796) compared to Sukomulyo (0.636). These findings suggest that elevation may influence yeast populations within honeycombs, with potential interactions with other factors affecting diversity measures.
Received 06/10/2023
Revised 20/02/2024
Accepted 22/02/2024
Published Online First 20/04/2024
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
How to Cite
References
Muslim T. Potensi Madu Hutan Sebagai Obat dan Pengelolaannya di Indonesia. InProsiding Seminar Balitek KSDA 2014 Dec (pp. 67-87). https://www.mendeley.com/catalogue/88fac00d-a813-3a1d-829d-39394d358d00/
Robinson WS. Surfing the sweet wave: migrating giant honey bees (Hymenoptera: Apidae: Apis dorsata) display spatial and temporal fidelity to annual stopover site in Thailand. J Insect Sci. 2021 Nov; 21(6): 1. https://doi.org/10.1093/jisesa/ieab037
Eckert JE. The flight range of the honeybee. J Agric Res. 1933; 47(5): 257–85. Available from : Eckert-Flight-Range-of-the-Honey-Bee.pdf (theapiarist.org).
Skorbiłowicz E, Skorbiłowicz M, Ciesluk I. Bees as bioindicators of environmental pollution with metals in an urban area. J Ecol Eng. 2018; 19(3): 229–34. https://doi.org/10.12911/22998993/85738
Hristov P, Shumkova R, Palova N, Neov B. Factors associated with honey bee colony losses: a mini-review. Vet Sci. 2020 Oct 30;7(4):166. https://doi.org/10.3390/vetsci7040166
Xiong ZR, Sogin JH, Worobo RW. Microbiome analysis of raw honey reveals important factors influencing the bacterial and fungal communities. Front Microbiol. 2023 Jan 12; 13: 1099522. https://doi.org/10.3389/fmicb.2022.1099522
Kogan H V, Elikan AB, Glaser KF, Bergmann JM, Raymond LM, Prado-Irwin SR, et al. Colonization of honey bee digestive tracts by environmental yeast Lachancea thermotolerans is naturally occurring, temperature dependent, and impacts the microbiome of newly emerged bees . Microbiol Spectr. 2023; 11(2): e05194-22. https://doi.org/10.1128/spectrum.05194-22
Snowdon JA, Cliver DO. Microorganisms in honey. Int J Food Microbiol. 1996; 31(1–3): 1–26. https://doi.org/10.1016/0168-1605(96)00970-1
Echeverrigaray S, Scariot FJ, Foresti L, Schwarz LV, Rocha RKM, da Silva GP, et al. Yeast biodiversity in honey produced by stingless bees raised in the highlands of southern Brazil. Int J Food Microbiol. 2021 April; 347: 109200. https://doi.org/10.1016/j.ijfoodmicro.2021.109200
Boekhout T, Amend AS, El Baidouri F, Gabaldón T, Geml J, Mittelbach M, et al. Trends in yeast diversity discovery. Fungal Diversity. 2022 May; 114: 491–537. https://doi.org/10.1007/s13225-021-00494-6
Rosa CA, Lachance MA, Limtong S, Santos ARO, Landell MF, et al. Yeasts from tropical forests: biodiversity, ecological interactions, and as sources of bioinnovation. Yeast. 2023 Nov; 40(11): 511-39. https://doi.org/10.1002/yea.3903
Christmann, T, Menor, IO. A synthesis and future research directions for tropical mountain ecosystem restoration. Sci Rep. 2021 Dec; 11: 23948. https://doi.org/10.1038/s41598-021-03205-y
Prayitno Y., Emmawati A, Rahmadi A. Physico-chemical characteristics, antibacterial, and antioxidant activities of genuine forest honey from East Kalimantan. Food Res. 2020 Aug; 4(6): 1969–78. http://dx.doi.org/10.26656/fr.2017.4(6).235
Riswahyuli Y, Rohman A, Setyabudi FMCS, Raharjo S. Evaluation of phenolic content and free radical scavenging activity of Indonesia wild honey collected from seven different regions. J Food Res. 2019 Oct; 8(6): 94-103. https://doi.org/10.5539/jfr.v8n6p94
Riswahyuli Y, Rohman A, Setyabudi FMCS, Raharjo S. Characterization of Indonesia wild honey and its potential for authentication and origin distinction. Food Res. 2020 Jun; 4(5): 1670–80. https://doi.org/10.26656/fr.2017.4(5).105
Moreira GAM, Mangaravite É, Vieira NM, Silveira FA da, Silveira WB da, Vale HMM do. Yeast species and strains differing along an altitudinal gradient in the Brazilian forest domain. Rev Bras Ciênc Solo. 2020 Nov; 44: e0200033. https://doi.org/10.36783/18069657rbcs20200033
Yahyapour G, Anvar SAA, Ataee M, Ahari Hamed H, Askari H. Isolation, identification, and characterization of the native yeast strains from homemade cheese to assess their eliminating impact on the aflatoxin B1 and M1 of the simulated gastrointestinal fluid. Iran J Biotechnol. 2023 Apr 1; 21(2): e3291. https://doi.org/10.30498/ijb.2023.330834.3291
Hall T. BioEdit: An important software for molecular biology. GERF Bull Biosci. 2011; 2(June): 60–1.
Koichiro T, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol. 2021 Jul; 38 (7): 3022-3027. https://doi.org/10.1093/molbev/msab120
Xu J. Fungal DNA barcoding. Genome. 2016 Nov; 59 (11) : 913–32. https://doi.org/10.1139/gen-2016-0046
Aljohani R, Samarasinghe H, Ashu T, Xu J. Diversity and relationships among strains of culturable yeasts in agricultural soils in Cameroon. Sci Rep. 2018 Oct; 8: 15687. https://doi.org/10.1038/s41598-018-34122-2
Reinoso S, Gutiérrez MS, Domínguez-Borbor C, Argüello-Guevara W, Bohórquez-Cruz M, Sonnenholzner S, et al. Selection of autochthonous yeasts isolated from the intestinal tracts of cobia fish (Rachycentron canadum) with probiotic potential. J Fungi (Basel). 2023 Feb 18; 9(2): 274. https://doi.org/10.3390/jof9020274
Heras J, Domínguez C, Mata E, Pascual V, Lozano C, Torres C, et al. GelJ-a tool for analyzing DNA fingerprint gel images. BMC Bioinformatics. 2015 Aug 26; 16: 270. https://doi.org/10.1186/s12859-015-0703-0
Rohlf FJ R. NTSYS-pc, numerical taxonomy and multivariate analysis system version 2.1. 2009. New York, USA: Exeter Software.
Siavoshi F, Sahraee M, Ebrahimi H, Sarrafnejad A, Saniee P. Natural fruits, flowers, honey, and honeybees harbor Helicobacter pylori-positive yeasts. Helicobacter. 2018 Apr; 23(2): e12471. https://doi.org/10.1111/hel.12471
Rossi F, Torriani S. Debaryomyces. In: Liu D, editor. Handbook of foodborne diseases. Boca Raton: Taylor & Francis; 2019.p. 473-490. https://doi.org/10.1111/hel.1247110.1201/b22030
Martinez SJ, Simão JBP, Pylro VS, Schwan RF. The altitude of coffee cultivation causes shifts in the microbial community assembly and biochemical compounds in natural induced anaerobic fermentations. Front Microbiol. 2021 May 20;12: 671395. https://doi.org/10.1111/hel.1247110.3389/fmicb.2021.671395
Kurtzman CP. Priceomyces. In: Kurtzman CP, Fell JW, Boekhout T, editors. The Yeasts : a taxonomic study. 5th ed. Elsevier B.V.; 2011. p.719–24. https://doi.org/10.1111/hel.1247110.1016/B978-0-444-52149-1.00059-8
Kanpiengjai A, Kodchasee P, Unban K, Kumla J, Lumyong S, Khunnamwong P, et al. Three new yeast species from flowers of Camellia sinensis var. assamica collected in Northern Thailand and their tannin tolerance characterization. Front Microbiol. 2023 Feb 16; 14: 1043430. https://doi.org/10.1111/hel.1247110.3389/fmicb.2023.1043430
Yurkov A. Temporal and geographic patterns in yeast distribution. In: Buzzini P, Lachance MA, Yurkov A, editors. Yeasts in natural ecosystems: ecology. Springer International Publishing; 2017. p. 101–30. https://doi.org/10.1007/978-3-319-61575-2
Inácio CP, Diniz M V., Araújo PSR, Barros MS, Andrade MCL, Lima-Neto RG, et al. Bloodstream infection of a cancer patient by Cystobasidium minutum: a case report and literature review. Mycopathologia. 2020 Apr; 185(2): 395-98. https://doi.org/10.1007/s11046-019-00415-x
Borman AM, Johnson EM. Changes in fungal taxonomy: mycological rationale and clinical implications. Clin Microbiol Rev. 2023 Dec 20; 36(4): e0009922. https://doi.org/10.1128/cmr.00099-22
Gowthami G, Gunashree B S. Isolation, characterization and optimization of Cystobasidium minutum for phytase production. Biomedicine. 2023 Feb ; 43(1): 329–34. https://doi.org/10.51248/.v43i01.2654
Valsalan, R, Mathew, D. Draft genome of Meyerozyma guilliermondii strain vka1: a yeast strain with composting potential. J Genet Eng Biotechnol. 2020; 18(1): 54. https://doi.org/10.1186/s43141-020-00074-2
Francisco EC, Ribeiro FdC, Junior JNA, Betto Pedoni DB, da Matta DA, Dolande M, et al. Emergence of cryptic species and clades of Meyerozyma guilliermondii species complex exhibiting limited in vitro susceptibility to antifungals in patients with candidemia. Microbiol Spectr. 2023 Sept 12; 11(5): e05115-22. https://doi.org/10.1128/spectrum.05115-22
Zahoor F, Sooklim C, Songdech P, Duangpakdee O, Soontorngun N. Selection of potential yeast probiotics and a cell factory for xylitol or acid production from honeybee samples. Metabolites. 2021 May 13; 11(5): 312. https://doi.org/10.3390/metabo11050312
Nakase T, Jindamorakot S, Am-In S, Potacharoen W, Tanticharoen M. Yeast biodiversity in tropical forests of Asia. In: Péter G, Rosa C, editors. The yeast handbook : biodiversity and ecophysiology of yeasts. 1st ed. Springer Berlin, Heidelberg; 2006. p. 441–60. https://doi.org/10.1007/3-540-30985-3
Huang Z, Su Y, Lin S, Wu G, Cheng H, Huang G. Elevational patterns of microbial species richness and evenness across climatic zones and taxonomic scales. Ecol Evol. 2023 Oct 9; 13(10): e10594. https://doi.org/10.1002/ece3.10594
Ohdo T, Takahashi K. Plant species richness and community assembly along gradients of elevation and soil nitrogen availability. AoB PLANTS. 2020 Jun; 12(3): plaa014. https://doi.org/10.1093/aobpla/plaa014
Türk G, Şen K. Changes of various quality characteristics and aroma compounds of astragalus honey obtained from different altitudes of Adana-Turkey. J Food Process Preserv. 2021; 45(10): e15852. https://doi.org/10.1111/jfpp.15852.
Conrad KM, Peters VE, Rehan SM. Tropical bee species abundance differs within a narrow elevational gradient. Sci Rep. 2021 Dec; 11(1): 23368. https://doi.org/10.1038/s41598-021-02727-9.