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Open AccessArticle

Amplicon Sequencing of Variable 16S rRNA from Bacteria and ITS2 Regions from Fungi and Plants, Reveals Honeybee Susceptibility to Diseases Results from Their Forage Availability under Anthropogenic Landscapes

1
Department of Immunobiology, Faculty of Biology and Biotechnology, Institute of Biological Sciences, Maria Curie-Skłodowska University, Akademicka 19 Str., 20-033 Lublin, Poland
2
School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK
3
Polish-Japanese Academy of Information Technology, Koszykowa 86 Str., 02-008 Warsaw, Poland
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Laboratory of Gene Expression, ECOTECH-Complex, Maria Curie-Sklodowska University, ul. Gleboka 39, 20-612 Lublin, Poland
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Department of Life Sciences, Insects Division, Natural History Museum, London SW7 5BD, UK
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Biobank Lab, Department of Molecular Biophysics, Faculty of Biology and Environmental Protection, University of Łódź, Pilarskiego 14/16, 90-231 Łódź, Poland
7
Department of Veterinary Microbiology, Faculty of Veterinary Medicine, Institute of Preclinical Veterinary Sciences, University of Life Sciences, Akademicka 12, 20-033 Lublin, Poland
8
Department of Pharmaceutical Botany and Pharmacognosy, Ludwik Rydygier Collegium Medicum, Nicolaus Copernicus University, Marie Curie-Skłodowska 9, 85-094 Bydgoszcz, Poland
9
Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4 Str., 20-290 Lublin, Poland
10
Faculty of Production and Power Engineering, University of Agriculture in Kraków, Balicka 116B, 30-149 Kraków, Poland
11
Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand
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Research Center of Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
13
Centro de Investigación Apícola y Agroambiental (CIAPA), Laboratorio de Patología Apícola, IRIAF Instituto Regional de Investigación y Desarrollo Agroalimentario y Forestal, Consejería de Agricultura de la Junta de Comunidades de Castilla-La Mancha, Camino de San Martín s/n, 19180 Marchamalo, Spain
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Instituto de Recursos Humanos para la Ciencia y la Tecnología (INCRECYT-FEDER), Fundación Parque Científico y Tecnológico de Castilla—La Mancha, 02006 Albacete, Spain
15
Department of Molecular Biology, Institute of Biological Sciences, Maria Curie-Sklodowska University, Akademicka 19 Str., 20-033 Lublin, Poland
*
Author to whom correspondence should be addressed.
Senior author.
Academic Editor: Giovanni Cilia
Pathogens 2021, 10(3), 381; https://doi.org/10.3390/pathogens10030381
Received: 22 January 2021 / Revised: 17 March 2021 / Accepted: 18 March 2021 / Published: 22 March 2021
(This article belongs to the Special Issue Infection in Honey Bees: Host–Pathogen Interaction and Spillover)
European Apis mellifera and Asian Apis cerana honeybees are essential crop pollinators. Microbiome studies can provide complex information on health and fitness of these insects in relation to environmental changes, and plant availability. Amplicon sequencing of variable regions of the 16S rRNA from bacteria and the internally transcribed spacer (ITS) regions from fungi and plants allow identification of the metabiome. These methods provide a tool for monitoring otherwise uncultured microbes isolated from the gut of the honeybees. They also help monitor the composition of the gut fungi and, intriguingly, pollen collected by the insect. Here, we present data from amplicon sequencing of the 16S rRNA from bacteria and ITS2 regions from fungi and plants derived from honeybees collected at various time points from anthropogenic landscapes such as urban areas in Poland, UK, Spain, Greece, and Thailand. We have analysed microbial content of honeybee intestine as well as fungi and pollens. Furthermore, isolated DNA was used as the template for screening pathogens: Nosema apis, N. ceranae, N. bombi, tracheal mite (Acarapis woodi), any organism in the parasitic order Trypanosomatida, including Crithidia spp. (i.e., Crithidia mellificae), neogregarines including Mattesia and Apicystis spp. (i.e., Apicistis bombi). We conclude that differences between samples were mainly influenced by the bacteria, plant pollen and fungi, respectively. Moreover, honeybees feeding on a sugar based diet were more prone to fungal pathogens (Nosema ceranae) and neogregarines. In most samples Nosema sp. and neogregarines parasitized the host bee at the same time. A higher load of fungi, and bacteria groups such as Firmicutes (Lactobacillus); γ-proteobacteria, Neisseriaceae, and other unidentified bacteria was observed for Nosema ceranae and neogregarine infected honeybees. Healthy honeybees had a higher load of plant pollen, and bacteria groups such as: Orbales, Gilliamella, Snodgrassella, and Enterobacteriaceae. Finally, the period when honeybees switch to the winter generation (longer-lived forager honeybees) is the most sensitive to diet perturbations, and hence pathogen attack, for the whole beekeeping season. It is possible that evolutionary adaptation of bees fails to benefit them in the modern anthropomorphised environment. View Full-Text
Keywords: Apis mellifera; 16S rRNA; ITR2; NGS; Nosema apis; Nosema ceranae; Nosema bombi; Acarapis woodi; Trypanosomatida; Crithidia spp.; neogregarines; Apicystis spp.; antropocene; insectageddon; urban area; urban environment; bee biology Apis mellifera; 16S rRNA; ITR2; NGS; Nosema apis; Nosema ceranae; Nosema bombi; Acarapis woodi; Trypanosomatida; Crithidia spp.; neogregarines; Apicystis spp.; antropocene; insectageddon; urban area; urban environment; bee biology
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MDPI and ACS Style

Ptaszyńska, A.A.; Latoch, P.; Hurd, P.J.; Polaszek, A.; Michalska-Madej, J.; Grochowalski, Ł.; Strapagiel, D.; Gnat, S.; Załuski, D.; Gancarz, M.; Rusinek, R.; Krutmuang, P.; Martín Hernández, R.; Higes Pascual, M.; Starosta, A.L. Amplicon Sequencing of Variable 16S rRNA from Bacteria and ITS2 Regions from Fungi and Plants, Reveals Honeybee Susceptibility to Diseases Results from Their Forage Availability under Anthropogenic Landscapes. Pathogens 2021, 10, 381. https://doi.org/10.3390/pathogens10030381

AMA Style

Ptaszyńska AA, Latoch P, Hurd PJ, Polaszek A, Michalska-Madej J, Grochowalski Ł, Strapagiel D, Gnat S, Załuski D, Gancarz M, Rusinek R, Krutmuang P, Martín Hernández R, Higes Pascual M, Starosta AL. Amplicon Sequencing of Variable 16S rRNA from Bacteria and ITS2 Regions from Fungi and Plants, Reveals Honeybee Susceptibility to Diseases Results from Their Forage Availability under Anthropogenic Landscapes. Pathogens. 2021; 10(3):381. https://doi.org/10.3390/pathogens10030381

Chicago/Turabian Style

Ptaszyńska, Aneta A.; Latoch, Przemyslaw; Hurd, Paul J.; Polaszek, Andrew; Michalska-Madej, Joanna; Grochowalski, Łukasz; Strapagiel, Dominik; Gnat, Sebastian; Załuski, Daniel; Gancarz, Marek; Rusinek, Robert; Krutmuang, Patcharin; Martín Hernández, Raquel; Higes Pascual, Mariano; Starosta, Agata L. 2021. "Amplicon Sequencing of Variable 16S rRNA from Bacteria and ITS2 Regions from Fungi and Plants, Reveals Honeybee Susceptibility to Diseases Results from Their Forage Availability under Anthropogenic Landscapes" Pathogens 10, no. 3: 381. https://doi.org/10.3390/pathogens10030381

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