Abstract
Bee gut microbial communities have been studied extensively and linked to honey bee biology in terms of stages of bee development and behavior. Associations of bee gut microbiota in health and disease have also been explored. A large number of studies have centered on the gut microbiome of Apis mellifera, with similar investigations lagging far behind in Asian honey bee foragers. In this study, we characterized and compared the gut bacterial profiles of foragers and nurse bees of A. cerana and A. mellifera. Analysis of 16S rRNA partial gene sequences revealed significant differences in gut bacterial communities between the two honey bee species. Despite sharing dominant taxa, Bacteroides was more abundant in A. cerana, while Proteobacteria was higher in A. mellifera. Specific gut members are distinctly associated with hosts performing different tasks (i.e. nurse bees versus foragers). An exclusive abundance of Apibacter detected in Asian honey bee seemed to be a microbial signature of A. cerana foragers. Overall, our study highlights that variations in gut microbiota could be linked to task-specific (nurse bees and foragers) bacterial species associated with honey bees. Future investigations on the symbiotic relationship between host and the resident microbiota would be beneficial for improving honey bee health.
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Availability of data and material
The raw reads of 16S rRNA genes of honey bee gut microbiome generated during the current study have been deposited at the [NCBI Sequence Read Archive (SRA)] database under the Bioproject accession number PRJNA636089 (the BioSample accession numbers SAMN15063615-SAMN15063630) [https://www.ncbi.nlm.nih.gov/bioproject/PRJNA636089].
Abbreviations
- AC:
-
Asian hive bees (A. cerana).
- AM:
-
European farm bees (A. mellifera).
- AC.N:
-
Asian A. cerana nurse bees
- AC.F:
-
Asian A. cerana foragers
- AM.N:
-
European A. mellifera nurse bees
- AM.F:
-
European A. mellifera foragers
References
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. https://doi.org/10.1111/j.1541-0420.2005.00440.x
Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. https://doi.org/10.1111/j.1461-0248.2006.00926.x
Asnicar F, Weingart G, Tickle TL et al (2015) Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ 2015:e1029–e1029. https://doi.org/10.7717/peerj.1029
Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. https://doi.org/10.1038/nmeth.2276
Bonilla-Rosso G, Engel P (2018) Functional roles and metabolic niches in the honey bee gut microbiota. Curr Opin Microbiol 43:69–76. https://doi.org/10.1016/j.mib.2017.12.009
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Carreck NL, Andree M, Brent CS et al (2013) Standard methods for Apis mellifera anatomy and dissection. J Apic Res 52:1–40
Corby-Harris V, Maes P, Anderson KE (2014) The bacterial communities associated with honey bee (apis mellifera) foragers. PLOS ONE. https://doi.org/10.1371/journal.pone.0095056
Corby-Harris V, Snyder L, Meador C, Ayotte T (2018) Honey bee (Apis mellifera) nurses do not consume pollens based on their nutritional quality. PLoS ONE 13:e0191050–e0191050. https://doi.org/10.1371/journal.pone.0191050
D’Alvise P, Böhme F, Codrea MC et al (2018) The impact of winter feed type on intestinal microbiota and parasites in honey bees. Apidologie 49:252–264. https://doi.org/10.1007/s13592-017-0551-1
Disayathanoowat T, Young JPW, Helgason T, Chantawannakul P (2012) T-RFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand. FEMS Microbiol Ecol 79:273–281. https://doi.org/10.1111/j.1574-6941.2011.01216.x
Disayathanoowat T, Li H, Supapimon N et al (2020) Different dynamics of bacterial and fungal communities in hive-stored bee bread and their possible roles: a case study from two commercial honey bees in China. Microorganisms 8:264. https://doi.org/10.3390/microorganisms8020264
Duong BTT, Lien NTK, Thu HT et al (2020) Investigation of the gut microbiome of Apis cerana honeybees from Vietnam. Biotechnol Lett 42:2309–2317. https://doi.org/10.1007/s10529-020-02948-4
Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Ellegaard KM, Engel P (2019) Genomic diversity landscape of the honey bee gut microbiota. Nat Commun 10:446. https://doi.org/10.1038/s41467-019-08303-0
Ellegaard KM, Suenami S, Miyazaki R, Engel P (2020) Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species. Curr Biol 30:2520-2531.e7. https://doi.org/10.1016/j.cub.2020.04.070
Emery O, Schmidt K, Engel P (2017) Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Mol Ecol 26:2576–2590. https://doi.org/10.1111/mec.14058
Engel P, Moran NA (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiol Rev 37:699–735
Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci USA 109:11002–11007. https://doi.org/10.1073/pnas.1202970109
Engel P, Kwong WK, McFrederick Q et al (2016) The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions. Mbio 7:e02164-e2215. https://doi.org/10.1128/mBio.02164-15
Haas BJ, Gevers D, Earl AM et al (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504. https://doi.org/10.1101/gr.112730.110
Jones JC, Fruciano C, Marchant J et al (2018) The gut microbiome is associated with behavioural task in honey bees. Insectes Soc 65:419–429. https://doi.org/10.1007/s00040-018-0624-9
Kešnerová L, Mars RAT, Ellegaard KM et al (2017) Disentangling metabolic functions of bacteria in the honey bee gut. PLOS Biol. https://doi.org/10.1371/journal.pbio.2003467
Kešnerová L, Emery O, Troilo M et al (2020) Gut microbiota structure differs between honeybees in winter and summer. ISME J 14:801–814. https://doi.org/10.1038/s41396-019-0568-8
Khan KA, Ansari MJ, Al-Ghamdi A et al (2017) Investigation of gut microbial communities associated with indigenous honey bee (Apis mellifera jemenitica) from two different eco-regions of Saudi Arabia. Saudi J Biol Sci 24:1061–1068. https://doi.org/10.1016/j.sjbs.2017.01.055
Klindworth A, Pruesse E, Schweer T et al (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1. https://doi.org/10.1093/nar/gks808
Kwong WK (2020) Microbiome evolution: having the guts to be different. Curr Biol 30:R766–R768. https://doi.org/10.1016/j.cub.2020.05.040
Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384
Kwong WK, Medina LA, Koch H et al (2017) Dynamic microbiome evolution in social bees. Sci Adv 3:e1600513. https://doi.org/10.1126/sciadv.1600513
Kwong WK, Steele MI, Moran NA (2018) Genome sequences of Apibacter spp., gut symbionts of asian honey bees. Genome Biol Evol 10:1174–1179. https://doi.org/10.1093/gbe/evy076
Lee FJ, Miller KI, McKinlay JB, Newton ILG (2018) Differential carbohydrate utilization and organic acid production by honey bee symbionts. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiy113
Luo Z-W, Dong Z-X, Chen Y-F et al (2020) Comparative analysis of the gut microbiota of Apis cerana in Yunnan using high-throughput sequencing. Arch Microbiol 202:2557–2567. https://doi.org/10.1007/s00203-020-01974-0
Maes PW, Rodrigues PAP, Oliver R et al (2016) Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Mol Ecol 25:5439–5450. https://doi.org/10.1111/mec.13862
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
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–e36393. https://doi.org/10.1371/journal.pone.0036393
Oksanen J, Kindt R, Pierre L, et al. Vegan: Community Ecology Package, R package version 2.4–0. R Packag. version 2.2–1; 2016.
Park D, Jung JW, Choi B-S et al (2015) Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing. BMC Genom. https://doi.org/10.1186/1471-2164-16-1
Powell JE, Martinson VG, Urban-Mead K, Moran NA (2014) Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl Environ Microbiol 80:7378–7387. https://doi.org/10.1128/AEM.01861-14
Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Raymann K, Moran NA (2018) The role of the gut microbiome in health and disease of adult honey bee workers. Curr Opin Insect Sci 26:97–104. https://doi.org/10.1016/j.cois.2018.02.012
Rothman JA, Carroll MJ, Meikle WG et al (2018) Longitudinal effects of supplemental forage on the honey bee (Apis mellifera) microbiota and inter- and intra-colony variability. Microb Ecol 76:814–824. https://doi.org/10.1007/s00248-018-1151-y
Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
Taylor MA, Robertson AW, Biggs PJ et al (2019) The effect of carbohydrate sources: sucrose, invert sugar and components of mānuka honey, on core bacteria in the digestive tract of adult honey bees (Apis mellifera). PLOS ONE 14:e0225845. https://doi.org/10.1371/journal.pone.0225845
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang H, Liu C, Liu Z et al (2020) The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering. BMC Microbiol 20:61. https://doi.org/10.1186/s12866-020-01726-6
White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5:e1000352–e1000352. https://doi.org/10.1371/journal.pcbi.1000352
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge
Wu Y, Zheng Y, Wang S et al (2021) Genetic divergence and functional convergence of gut bacteria between the Eastern honey bee Apis cerana and the Western honey bee Apis mellifera. J Adv Res. https://doi.org/10.1016/j.jare.2021.08.002
Zheng H, Nishida A, Kwong WK et al (2016) Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. Mbio 7:e01326-e1416. https://doi.org/10.1128/mBio.01326-16
Acknowledgements
The authors would like to thank Ms. Nantinee Moontan for technical assistance.
Funding
This work was financially supported by the [National Research Council of Thailand] (Grant Number [622B01057]) and [Mae Fah Luang University].
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KK and SP contributed to the study conception and design. Material preparation and data collection were performed by KK and SP. LG analyzed data. The first draft of the manuscript was written by LG, EG, KK, and SP. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Communicated by Erko Stackebrandt.
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Gruneck, L., Gentekaki, E., Khongphinitbunjong, K. et al. Distinct gut microbiota profiles of Asian honey bee (Apis cerana) foragers. Arch Microbiol 204, 187 (2022). https://doi.org/10.1007/s00203-022-02800-5
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DOI: https://doi.org/10.1007/s00203-022-02800-5