[en] Species traits and environmental conditions are among the many factors that shape bee communities. Their effective conservation is currently challenged due to global changes. The gut microbiome likely contributes to bee plasticity and resilience but is largely understudied in solitary bees. A stable core microbiome in social bees has been identified to be important for health and survival in changing environmental conditions, but knowledge on a host-specific core microbiome in solitary bees is very scarce. In the present study, we analyzed the gut bacterial and fungal communities of eight solitary bee species commonly found in apple orchards along a latitudinal gradient throughout Europe. We aimed to understand the intra- and interspecific variations in the gut microbial communities and the extent to which host species and local environment shape the solitary bee gut microbiota. The bacterial community showed strong host effects, with each bee species having a distinct core bacterial community that was mostly stable across locations. The fungal community was most strongly influenced by the local environment, while different environmental variables were responsible for the variation in bacterial and fungal communities. Our study demonstrated that the examined solitary bee species harbor a distinct microbial diversity and composition, which undergoes host- and location-specific filtering.
Disciplines :
Microbiology Environmental sciences & ecology
Author, co-author :
Hettiarachchi, Amanda; Department of Biochemistry and Microbiology, Faculty of Sciences, Laboratory of Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium
Tuerlings, Tina; Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Laboratory of Agrozoology, Coupure Links 653, 9000, Ghent, Belgium
Weekers, Timothy; Agroecology Lab, Université Libre de Bruxelles, Boulevard du Triomphe CP 264/02, 1050, Brussels, Belgium
Marshall, Leon; Agroecology Lab, Université Libre de Bruxelles, Boulevard du Triomphe CP 264/02, 1050, Brussels, Belgium ; Naturalis Biodiversity Center, Leiden, Netherlands
Leclercq, Nicolas ; Université de Liège - ULiège > Département GxABT > Biodiversité, Ecosystème et Paysage (BEP) ; Agroecology Lab, Université Libre de Bruxelles, Boulevard du Triomphe CP 264/02, 1050, Brussels, Belgium
Wood, Thomas James; Naturalis Biodiversity Center, Leiden, Netherlands ; Laboratory of Zoology, Research Institute for Biosciences, University of Mons, Place du Parc 20, 7000, Mons, Belgium
Cejas, Diego; Laboratory of Zoology, Research Institute for Biosciences, University of Mons, Place du Parc 20, 7000, Mons, Belgium
Gerard, Maxence; Laboratory of Zoology, Research Institute for Biosciences, University of Mons, Place du Parc 20, 7000, Mons, Belgium ; INSECT Lab, Division of Functional Morphology, Department of Zoology, Stockholm University, Svante Arrhenius väg 18b, 11418, Stockholm, Sweden
Vereecken, Nicolas J; Agroecology Lab, Université Libre de Bruxelles, Boulevard du Triomphe CP 264/02, 1050, Brussels, Belgium
Michez, Denis; Laboratory of Zoology, Research Institute for Biosciences, University of Mons, Place du Parc 20, 7000, Mons, Belgium
Smagghe, Guy; Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Laboratory of Agrozoology, Coupure Links 653, 9000, Ghent, Belgium
Joossens, Marie; Department of Biochemistry and Microbiology, Faculty of Sciences, Laboratory of Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium
Vandamme, Peter; Department of Biochemistry and Microbiology, Faculty of Sciences, Laboratory of Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium. Peter.Vandamme@ugent.be
FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen F.R.S.-FNRS - Fonds de la Recherche Scientifique
Funding text :
This study was funded by the Fonds Wetenschappelijk Onderzoek (FWO) and Fonds De La Recherche Scientifique (F.R.S.-FNRS) joint program Excellence of Science (EOS) for the project \u201CClimate change and its effects on pollination services\u201D (CliPS, project number 3094785).
T. Pievani The sixth mass extinction: Anthropocene and the human impact on biodiversity Rend Lincei 25 85 93 10.1007/s12210-013-0258-9
D.L. Wagner E.M. Grames M.L. Forister et al. Insect decline in the Anthropocene: death by a thousand cuts Proc Natl Acad Sci U S A 10.1073/pnas.2023989118 34876524 8685691
M. Gérard M. Vanderplanck T. Wood D. Michez Global warming and plant–pollinator mismatches Emerg Top Life Sci 4 77 86 10.1042/ETLS20190139 32558904 7326340
O. Schweiger J. Settele O. Kudrna et al. Climate change can cause spatial mismatch of trophically interacting species Ecology 10.1890/07-1748.1 19137952
Potts SG, Biesmeijer JC, Kremen C, et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25
M.M. Hofmann C.M. Zohner S.S. Renner Narrow habitat breadth and late-summer emergence increases extinction vulnerability in Central European bees Proc R Soc Lond B Biol Sci 286 10.1098/rspb.2019.0316 20190316
Duchenne F, Thébault E, Michez D, et al (2020) Phenological shifts alter the seasonal structure of pollinator assemblages in Europe. Nat Ecol Evol 4. https://doi.org/10.1038/s41559-019-1062-4
G. Ghisbain M. Gérard T.J. Wood Expanding insect pollinators in the Anthropocene Biol Rev 10.1111/brv.12777 34288353
K. Maebe A. De Baets P. Vandamme Impact of intraspecific variation on measurements of thermal tolerance in bumble bees J Therm Biol 99 10.1016/j.jtherbio.2021.103002 34420633 103002
K. Maebe N.J. Vereecken N. Piot et al. The holobiont as a key to the adaptation and conservation of wild bees in the Anthropocene Front Ecol Evol 10.3389/fevo.2021.781470
P. Engel W.K. Kwong Q. McFrederick et al. The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions MBio 10.1128/mBio.02164-15 27803186 5090037
W.K. Kwong N.A. Moran Gut microbial communities of social bees Nat Rev Microbiol 10.1038/nrmicro.2016.43 27140688 5648345
E.V.S. Motta N.A. Moran The honeybee microbiota and its impact on health and disease Nat Rev Microbiol 22 122 137 1:CAS:528:DC%2BB3sXisFagsrrI 10.1038/s41579-023-00990-3 38049554
J. Liberti E.T. Frank T. Kay et al. Gut microbiota influences onset of foraging-related behavior but not physiological hallmarks of division of labor in honeybees MBio 10.1128/mbio.01034-24 39072646 11389387
J.E. Powell E.V.S. Motta J. Liberti et al. Lack of significant effect of gut microbiota on weight gain in newly emerged worker honeybee R Soc Open Sci 10.1098/rsos.242151 40144287 11937919
V. Kowallik A.S. Mikheyev Honey bee larval and adult microbiome life stages are effectively decoupled with vertical transmission overcoming early life perturbations MBio 10.1128/mBio.02966-21 34933445 8689520
K.M. Kapheim M.M. Johnson M. Jolley Composition and acquisition of the microbiome in solitary, ground-nesting alkali bees Sci Rep 10.1038/s41598-021-82573-x 34426595 8382693
M. Gilliam S.L. Buchmann B.J. Lorenz R.J. Schmalzel Bacteria belonging to the genus Bacillus associated with three species of solitary bees Apidologie 10.1051/apido:19900202
J. Lozo T. Berić A. Terzić-Vidojević et al. Microbiota associated with pollen, bee bread, larvae and adults of solitary bee Osmia cornuta (Hymenoptera: Megachilidae) Bull Entomol Res 10.1017/S0007485315000292 25895542
P. Graystock S.M. Rehan Q.S. McFrederick Hunting for healthy microbiomes: determining the core microbiomes of Ceratina, Megalopta, and Apis bees and how they associate with microbes in bee collected pollen Conserv Genet 10.1007/s10592-017-0937-7
Q.S. McFrederick J.M. Thomas J.L. Neff et al. Flowers and wild megachilid bees share microbes Microb Ecol 10.1007/s00248-016-0838-1 27592345
Q.S. McFrederick H.Q. Vuong J.A. Rothman Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers Int J Syst Evol Microbiol 10.1099/ijsem.0.002758 29648528
H. Cohen Q.S. McFrederick S.M. Philpott Environment shapes the microbiome of the blue orchard bee, Osmia lignaria Microb Ecol 10.1007/s00248-020-01549-y 32572535
Holley JC, Jackson MN, Pham AT, et al (2022) Carpenter bees (Xylocopa) harbor a distinctive gut microbiome related to that of honey bees and bumble bees. Appl Environ Microbiol 88. https://doi.org/10.1128/aem.00203-22
A. Hettiarachchi M. Cnockaert M. Joossens et al. The wild solitary bees Andrena vaga, Anthophora plumipes, Colletes cunicularius, and Osmia cornuta microbiota are host specific and dominated by endosymbionts and environmental microorganisms Microb Ecol 86 3013 3026 1:CAS:528:DC%2BB3sXitVKhsrfE 10.1007/s00248-023-02304-9 37794084
W.A. Shell S.M. Rehan Comparative metagenomics reveals expanded insights into intra- and interspecific variation among wild bee microbiomes Commun Biol 5 603 10.1038/s42003-022-03535-1 35715496 9205906
P.N. Nguyen S.M. Rehan The effects of urban land use gradients on wild bee microbiomes Front Microbiol 10.3389/fmicb.2022.992660 36466654 9716133
P.N. Nguyen S.M. Rehan Wild bee and pollen microbiomes across an urban–rural divide FEMS Microbiol Ecol 10.1093/femsec/fiad158 38037395
Q.S. McFrederick W.T. Wcislo M.C. Hout U.G. Mueller Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees FEMS Microbiol Ecol 10.1111/1574-6941.12302 24579829
Vuong HQ, Mcfrederick QS, Angert E (2019) Comparative genomics of wild bee and flower isolated Lactobacillus reveals potential adaptation to the bee host. Genome Biol Evol 11. https://doi.org/10.1093/gbe/evz136
A. Keller Q.S. McFrederick P. Dharampal S. Steffan Shawn B. Danforth BryanN S. Leonhardt SaraD (More than) hitchhikers through the network: the shared microbiome of bees and flowers Curr Opin Insect Sci 10.1016/j.cois.2020.09.007 32992041
T. Weekers L. Marshall N. Leclercq Dominance of honey bees is negatively associated with wild bee diversity in commercial apple orchards regardless of management practices Agric Ecosyst Environ 10.1016/j.agee.2021.107697
I. Snauwaert S.P. Roels F. Van Nieuwerburgh et al. Microbial diversity and metabolite composition of Belgian red-brown acidic ales Int J Food Microbiol 10.1016/j.ijfoodmicro.2015.12.009 26802571
B.J. Callahan P.J. McMurdie M.J. Rosen et al. DADA2: high-resolution sample inference from Illumina amplicon data Nat Methods 10.1038/nmeth.3869 27214047 4927377
M. Martin Cutadapt removes adapter sequences from high-throughput sequencing reads EMBnet J 17 10.14806/ej.17.1.200 10
McLaren MR, Callahan BJ (2021) Silva 138.1 prokaryotic SSU taxonomic training data formatted for DADA2. Zenodo 1
Abarenkov K, Zirk A, Piirmann T, et al (2021) UNITE general FASTA release for eukaryotes. Version 10.05.2021. UNITE Community.
P.J. McMurdie S. Holmes Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data PLoS ONE 8 1:CAS:528:DC%2BC3sXntVWht7w%3D 10.1371/journal.pone.0061217 23630581 3632530 e61217
Oksanen J, Blanchet FG, Friendly M, et al (2020) Package “vegan” Title Community Ecology Package Version 2.5–7. R 2.5.
T.J. Wood J.M. Holland D. Goulson Diet characterisation of solitary bees on farmland: dietary specialisation predicts rarity Biodivers Conserv 25 2655 2671 1:STN:280:DC%2BB38vhs12jtA%3D%3D 10.1007/s10531-016-1191-x 32355425 7175682
M. Haider S. Dorn C. Sedivy A. Müller Phylogeny and floral hosts of a predominantly pollen generalist group of mason bees (Megachilidae: Osmiini) Biol J Linn Soc 111 78 91 10.1111/bij.12186
Allen-Perkins A, Magrach A, Dainese M et al (2022). Ecology. https://doi.org/10.1002/ecy.3614
C. Sedivy A. Müller S. Dorn Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: evidence for physiological adaptations to digest pollen Funct Ecol 10.1111/j.1365-2435.2010.01828.x
P.W. Eckerter M. Albrecht F. Herzog M.H. Entling Floral resource distribution and fitness consequences for two solitary bee species in agricultural landscapes Basic Appl Ecol 65 1 15 10.1016/j.baae.2022.09.005
A. Voulgari-Kokota Q.S. McFrederick I. Steffan-Dewenter A. Keller Drivers, diversity, and functions of the solitary-bee microbiota Trends Microbiol 10.1016/j.tim.2019.07.011 31451346
S.S. Greenleaf N.M. Williams R. Winfree C. Kremen Bee foraging ranges and their relationship to body size Oecologia 153 589 596 10.1007/s00442-007-0752-9 17483965
J. Huang J. An J. Wu P.H. Williams Extreme food-plant specialisation in Megabombus bumblebees as a product of long tongues combined with short nesting seasons PLoS ONE 10 1:CAS:528:DC%2BC2MXhvFKnurvO 10.1371/journal.pone.0132358 26267382 4534414 e0132358
R.L. Vannette The floral microbiome: plant, pollinator, and microbial perspectives Annu Rev Ecol Evol Syst 10.1146/annurev-ecolsys-011720-013401
Michez D, Rasmont P, Terzo M, Vereecken NJ (2019) Bees of Europe. NAP Editions, Paris, France
P. Engel N.A. Moran The gut microbiota of insects - diversity in structure and function FEMS Microbiol Rev 10.1111/1574-6976.12025 23692388
M. Lenaerts S. Álvarez-Pérez C. de Vega et al. Rosenbergiella australoborealis sp. nov., Rosenbergiella collisarenosi sp. nov. and Rosenbergiella epipactidis sp. nov., three novel bacterial species isolated from floral nectar Syst Appl Microbiol 37 402 411 1:CAS:528:DC%2BC2cXnsVWlur8%3D 10.1016/j.syapm.2014.03.002 24794950
A.R.O. Santos M.P. Leon K.O. Barros et al. Starmerella camargoi f.a., sp. nov., Starmerella ilheusensis f.a., sp. nov., Starmerella litoralis f.a., sp. nov., Starmerella opuntiae f.a., sp. nov., Starmerella roubikii f.a., sp. nov. and Starmerella vitae f.a., sp. nov., isolated from flowers and bees, and transfer of related Candida species to the genus Starmerella as new combinations Int J Syst Evol Microbiol 10.1099/ijsem.0.002675 30168795
M.I. Pozo C.M. Herrera M.A. Lachance et al. Species coexistence in simple microbial communities: unravelling the phenotypic landscape of co-occurring Metschnikowia species in floral nectar Environ Microbiol 10.1111/1462-2920.13037 26337395
M.W. Silby C. Winstanley S.A.C. Godfrey Pseudomonas genomes: diverse and adaptable FEMS Microbiol Rev 10.1111/j.1574-6976.2011.00269.x 21361996
M. Wels R. Siezen S. Van Hijum Comparative genome analysis of Lactococcus lactis indicates niche adaptation and resolves genotype/phenotype disparity Front Microbiol 10.3389/fmicb.2019.00004 30766512 6365430
I. Iturrieta-González D. García J. Gené Novel species of Cladosporium from environmental sources in Spain MycoKeys 10.3897/mycokeys.77.60862 33510579 7803722
J.B. Parish E.S. Scott K. Hogendoorn Nutritional benefit of fungal spores for honey bee workers Sci Rep 10.1038/s41598-020-72758-1 33087805 7578645
D. Passerini M. Coddeville P. Le Bourgeois et al. The carbohydrate metabolism signature of Lactococcus lactis strain A12 reveals its sourdough ecosystem origin Appl Environ Microbiol 10.1128/AEM.01560-13 23872564 3811347
N. Kishimoto Y. Kosako N. Wakao et al. Transfer of Acidiphilium facilis and Acidiphilium aminolytica to the genus Acidocella gen. nov., and emendation of the genus Acidiphilium Syst Appl Microbiol 10.1016/S0723-2020(11)80453-4
Q.S. McFrederick W.T. Wcislo D.R. Taylor Environment or kin: whence do bees obtain acidophilic bacteria? Mol Ecol 10.1111/j.1365-294X.2012.05496.x 22340254
G.P. Smith H. Cohen J.F. Zorn Plant–pollinator network architecture does not impact intraspecific microbiome variability Mol Ecol 10.1111/mec.17306 39543938 11665498
