{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T18:51:19Z","timestamp":1792263079858,"version":"4.4.0"},"reference-count":90,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,11,17]],"date-time":"2021-11-17T00:00:00Z","timestamp":1637107200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,11,17]],"date-time":"2021-11-17T00:00:00Z","timestamp":1637107200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100012166","name":"national key r&d program of china","doi-asserted-by":"crossref","award":["2019YFA0906500"],"award-info":[{"award-number":["2019YFA0906500"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"national natural science foundation of china","doi-asserted-by":"publisher","award":["31870472"],"award-info":[{"award-number":["31870472"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Microbiome"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and \u201csequence-discrete population\u201d levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of <jats:italic>Snodgrassella alvi<\/jats:italic> are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of <jats:italic>Bifidobacterium<\/jats:italic> strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of <jats:italic>Bifidobacterium<\/jats:italic> with a specific polysaccharide utilization locus impacts the alternative splicing of the <jats:italic>gluR-B<\/jats:italic> gene, which is associated with an increased GABA level in the brain.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions.<\/jats:p>\n                \n              <\/jats:sec>","DOI":"10.1186\/s40168-021-01174-y","type":"journal-article","created":{"date-parts":[[2021,11,17]],"date-time":"2021-11-17T04:39:19Z","timestamp":1637123959000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":70,"title":["Honey bee genetics shape the strain-level structure of gut microbiota in social transmission"],"prefix":"10.1186","volume":"9","author":[{"given":"Jiaqiang","family":"Wu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haoyu","family":"Lang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohuan","family":"Mu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zijing","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qinzhi","family":"Su","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaosong","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3313-1675","authenticated-orcid":false,"given":"Hao","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,11,17]]},"reference":[{"key":"1174_CR1","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1146\/annurev-ecolsys-110617-062453","volume":"50","author":"NA Moran","year":"2019","unstructured":"Moran NA, Ochman H, Hammer TJ. Evolutionary and ecological consequences of gut microbial communities. Annu Rev Ecol Evol Syst. 2019;50:451\u201375.","journal-title":"Annu Rev Ecol Evol Syst"},{"key":"1174_CR2","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1038\/nature11053","volume":"486","author":"T Yatsunenko","year":"2012","unstructured":"Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222\u20137.","journal-title":"Nature."},{"key":"1174_CR3","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1038\/nrgastro.2017.29","volume":"14","author":"EMM Quigley","year":"2017","unstructured":"Quigley EMM. Gut microbiome as a clinical tool in gastrointestinal disease management: are we there yet? Nat Rev Gastroenterol Hepatol. 2017;14:315\u201320.","journal-title":"Nat Rev Gastroenterol Hepatol"},{"key":"1174_CR4","first-page":"4742","volume":"20","author":"S Bibbo","year":"2016","unstructured":"Bibbo S, Ianiro G, Giorgio V, Scaldaferri F, Masucci L, Gasbarrini A, et al. The role of diet on gut microbiota composition. Eur Rev Med Pharmacol Sci. 2016;20:4742\u20139.","journal-title":"Eur Rev Med Pharmacol Sci"},{"key":"1174_CR5","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1146\/annurev-genet-110711-155532","volume":"51","author":"JK Goodrich","year":"2017","unstructured":"Goodrich JK, Davenport ER, Clark AG, Ley RE. The relationship between the human genome and microbiome comes into view. Annu Rev Genet. 2017;51:413\u201333.","journal-title":"Annu Rev Genet"},{"key":"1174_CR6","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1128\/AEM.03301-15","volume":"82","author":"JM Chaston","year":"2016","unstructured":"Chaston JM, Dobson AJ, Newell PD, Douglas AE. Host genetic control of the microbiota mediates the Drosophila nutritional phenotype. Appl Environ Microbiol. 2016;82:671\u20139.","journal-title":"Appl Environ Microbiol"},{"key":"1174_CR7","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1016\/j.cell.2014.09.053","volume":"159","author":"JK Goodrich","year":"2014","unstructured":"Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. Human genetics shape the gut microbiome. Cell. 2014;159:789\u201399.","journal-title":"Cell."},{"key":"1174_CR8","doi-asserted-by":"publisher","first-page":"6440","DOI":"10.1038\/ncomms7440","volume":"6","author":"J Wang","year":"2015","unstructured":"Wang J, Kalyan S, Steck N, Turner LM, Harr B, Kunzel S, et al. Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome. Nat Commun. 2015;6:6440.","journal-title":"Nat Commun"},{"key":"1174_CR9","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1038\/ismej.2009.112","volume":"4","author":"C Zhang","year":"2010","unstructured":"Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 2010;4:232\u201341.","journal-title":"ISME J"},{"key":"1174_CR10","doi-asserted-by":"publisher","first-page":"11070","DOI":"10.1073\/pnas.0504978102","volume":"102","author":"RE Ley","year":"2005","unstructured":"Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070\u20135.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1174_CR11","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1016\/j.chom.2016.04.017","volume":"19","author":"JK Goodrich","year":"2016","unstructured":"Goodrich JK, Davenport ER, Beaumont M, Jackson MA, Knight R, Ober C, et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe. 2016;19:731\u201343.","journal-title":"Cell Host Microbe"},{"key":"1174_CR12","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/j.chom.2008.02.015","volume":"3","author":"PJ Turnbaugh","year":"2008","unstructured":"Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3:213\u201323.","journal-title":"Cell Host Microbe"},{"key":"1174_CR13","doi-asserted-by":"publisher","first-page":"1413","DOI":"10.1038\/ng.3693","volume":"48","author":"W Turpin","year":"2016","unstructured":"Turpin W, Espin-Garcia O, Xu W, Silverberg MS, Kevans D, Smith MI, et al. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat Genet. 2016;48:1413\u20137.","journal-title":"Nat Genet"},{"key":"1174_CR14","doi-asserted-by":"publisher","first-page":"1031","DOI":"10.1136\/gutjnl-2015-311326","volume":"66","author":"MY Lim","year":"2017","unstructured":"Lim MY, You HJ, Yoon HS, Kwon B, Lee JY, Lee S, et al. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut. 2017;66:1031\u20138.","journal-title":"Gut."},{"key":"1174_CR15","doi-asserted-by":"publisher","first-page":"572","DOI":"10.1016\/j.cels.2016.10.004","volume":"3","author":"H Xie","year":"2016","unstructured":"Xie H, Guo R, Zhong H, Feng Q, Lan Z, Qin B, et al. Shotgun Metagenomics of 250 adult twins reveals genetic and environmental impacts on the gut microbiome. Cell Syst. 2016;3:572\u201384 e3.","journal-title":"Cell Syst"},{"key":"1174_CR16","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1007\/s13238-018-0532-9","volume":"9","author":"J Wang","year":"2018","unstructured":"Wang J, Chen L, Zhao N, Xu X, Xu Y, Zhu B. Of genes and microbes: solving the intricacies in host genomes. Prot Cell. 2018;9:446\u201361.","journal-title":"Prot Cell"},{"key":"1174_CR17","doi-asserted-by":"publisher","first-page":"e36393","DOI":"10.1371\/journal.pone.0036393","volume":"7","author":"NA Moran","year":"2012","unstructured":"Moran NA, Hansen AK, Powell JE, Sabree ZL. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One. 2012;7:e36393.","journal-title":"PLoS One"},{"key":"1174_CR18","doi-asserted-by":"publisher","first-page":"e1600513","DOI":"10.1126\/sciadv.1600513","volume":"3","author":"WK Kwong","year":"2017","unstructured":"Kwong WK, Medina LA, Koch H, Sing KW, Soh EJY, Ascher JS, et al. Dynamic microbiome evolution in social bees. Sci Adv. 2017;3:e1600513.","journal-title":"Sci Adv"},{"key":"1174_CR19","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1038\/s41467-019-08303-0","volume":"10","author":"KM Ellegaard","year":"2019","unstructured":"Ellegaard KM, Engel P. Genomic diversity landscape of the honey bee gut microbiota. Nat Commun. 2019;10:446.","journal-title":"Nat Commun"},{"key":"1174_CR20","doi-asserted-by":"publisher","first-page":"2520","DOI":"10.1016\/j.cub.2020.04.070","volume":"30","author":"KM Ellegaard","year":"2020","unstructured":"Ellegaard KM, Suenami S, Miyazaki R, Engel P. Vast Differences in strain-level diversity in the gut microbiota of two closely related honey bee species. Curr Biol. 2020;30:2520\u201331 e7.","journal-title":"Curr Biol"},{"key":"1174_CR21","doi-asserted-by":"publisher","first-page":"2057","DOI":"10.1111\/mec.14434","volume":"27","author":"K Raymann","year":"2018","unstructured":"Raymann K, Bobay LM, Moran NA. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Mol Ecol. 2018;27:2057\u201366.","journal-title":"Mol Ecol"},{"key":"1174_CR22","doi-asserted-by":"publisher","first-page":"4461","DOI":"10.1111\/mec.13787","volume":"25","author":"E Powell","year":"2016","unstructured":"Powell E, Ratnayeke N, Moran NA. Strain diversity and host specificity in a specialized gut symbiont of honeybees and bumblebees. Mol Ecol. 2016;25:4461\u201371.","journal-title":"Mol Ecol"},{"key":"1174_CR23","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1038\/s41684-018-0173-x","volume":"47","author":"H Zheng","year":"2018","unstructured":"Zheng H, Steele MI, Leonard SP, Motta EVS, Moran NA. Honey bees as models for gut microbiota research. Lab Anim. 2018;47:317\u201325.","journal-title":"Lab Anim"},{"key":"1174_CR24","doi-asserted-by":"publisher","first-page":"4775","DOI":"10.1073\/pnas.1701819114","volume":"114","author":"H Zheng","year":"2017","unstructured":"Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci U S A. 2017;114:4775\u201380.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1174_CR25","doi-asserted-by":"publisher","first-page":"e01326","DOI":"10.1128\/mBio.01326-16","volume":"7","author":"H Zheng","year":"2016","unstructured":"Zheng H, Nishida A, Kwong WK, Koch H, Engel P, Steele MI, et al. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. mBio. 2016;7:e01326\u201316.","journal-title":"mBio."},{"key":"1174_CR26","doi-asserted-by":"publisher","first-page":"7378","DOI":"10.1128\/AEM.01861-14","volume":"80","author":"JE Powell","year":"2014","unstructured":"Powell JE, Martinson VG, Urban-Mead K, Moran NA. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl Environ Microbiol. 2014;80:7378\u201387.","journal-title":"Appl Environ Microbiol"},{"key":"1174_CR27","doi-asserted-by":"publisher","first-page":"e0123911","DOI":"10.1371\/journal.pone.0123911","volume":"10","author":"KM Kapheim","year":"2015","unstructured":"Kapheim KM, Rao VD, Yeoman CJ, Wilson BA, White BA, Goldenfeld N, et al. Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS One. 2015;10:e0123911.","journal-title":"PLoS One"},{"key":"1174_CR28","doi-asserted-by":"publisher","first-page":"e0118707","DOI":"10.1371\/journal.pone.0118707","volume":"10","author":"Z Hroncova","year":"2015","unstructured":"Hroncova Z, Havlik J, Killer J, Doskocil I, Tyl J, Kamler M, et al. Variation in honey bee gut microbial diversity affected by ontogenetic stage, age and geographic location. PLoS One. 2015;10:e0118707.","journal-title":"PLoS One"},{"key":"1174_CR29","doi-asserted-by":"publisher","first-page":"857","DOI":"10.3390\/insects3030857","volume":"3","author":"R Brodschneider","year":"2012","unstructured":"Brodschneider R, Arnold G, Hrassnigg N, Crailsheim K. Does patriline composition change over a honey bee queen\u02bcs lifetime? Insects. 2012;3:857\u201369.","journal-title":"Insects."},{"key":"1174_CR30","doi-asserted-by":"publisher","first-page":"985","DOI":"10.1093\/genetics\/108.4.985","volume":"108","author":"HH Laidlaw","year":"1984","unstructured":"Laidlaw HH, Page RE. Polyandry in Honey Bees (APIS MELLIFERA L.): Sperm utilization and intracolony genetic relationships. Genetics. 1984;108:985\u201397.","journal-title":"Genetics."},{"key":"1174_CR31","doi-asserted-by":"publisher","first-page":"e32962","DOI":"10.1371\/journal.pone.0032962","volume":"7","author":"HR Mattila","year":"2012","unstructured":"Mattila HR, Rios D, Walker-Sperling VE, Roeselers G, Newton IL. Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. PLoS One. 2012;7:e32962.","journal-title":"PLoS One"},{"key":"1174_CR32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3896\/IBRA.1.52.4.09","volume":"52","author":"SW Cobey","year":"2013","unstructured":"Cobey SW, Tarpy DR, Woyke J. Standard methods for instrumental insemination of Apis mellifera queens. J Apic Res. 2013;52:1\u201318.","journal-title":"J Apic Res"},{"key":"1174_CR33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3896\/IBRA.1.52.4.12","volume":"52","author":"KS Delaplane","year":"2015","unstructured":"Delaplane KS, van der Steen J, Guzman-Novoa E. Standard methods for estimating strength parameters of Apis mellifera colonies. J Apic Res. 2015;52:1\u201312.","journal-title":"J Apic Res"},{"key":"1174_CR34","doi-asserted-by":"publisher","first-page":"25909","DOI":"10.1073\/pnas.1916224116","volume":"116","author":"H Zheng","year":"2019","unstructured":"Zheng H, Perreau J, Powell JE, Han B, Moran NA. Division of labor in honey bee gut microbiota for plant polysaccharide digestion. Proc Natl Acad Sci U S A. 2019;116:25909\u201316.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1174_CR35","doi-asserted-by":"publisher","first-page":"e00731","DOI":"10.1128\/mSystems.00731-19","volume":"5","author":"MR Olm","year":"2020","unstructured":"Olm MR, Crits-Christoph A, Diamond S, Lavy A, Matheus Carnevali PB, Banfield JF. Consistent metagenome-derived metrics verify and delineate bacterial species boundaries. mSystems. 2020;5:e00731\u201319.","journal-title":"mSystems."},{"key":"1174_CR36","doi-asserted-by":"publisher","first-page":"1612","DOI":"10.1101\/gr.201863.115","volume":"26","author":"S Nayfach","year":"2016","unstructured":"Nayfach S, Rodriguez-Mueller B, Garud N, Pollard KS. An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Res. 2016;26:1612\u201325.","journal-title":"Genome Res"},{"key":"1174_CR37","doi-asserted-by":"publisher","first-page":"960","DOI":"10.15252\/msb.20177589","volume":"13","author":"PI Costea","year":"2017","unstructured":"Costea PI, Coelho LP, Sunagawa S, Munch R, Huertacepas J, Forslund K, et al. Subspecies in the global human gut microbiome. Mol Syst Biol. 2017;13:960.","journal-title":"Mol Syst Biol"},{"key":"1174_CR38","doi-asserted-by":"publisher","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","volume":"34","author":"S Chen","year":"2018","unstructured":"Chen S, Zhou Y, Chen Y, Jia G. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884\u2013i90.","journal-title":"Bioinformatics."},{"key":"1174_CR39","doi-asserted-by":"publisher","first-page":"1138","DOI":"10.1089\/cmb.2017.0096","volume":"24","author":"A Kechin","year":"2017","unstructured":"Kechin A, Boyarskikh U, Kel A, Filipenko M. cutPrimers: a new tool for accurate cutting of primers from reads of targeted next generation sequencing. J Comput Biol. 2017;24:1138\u201343.","journal-title":"J Comput Biol"},{"key":"1174_CR40","first-page":"5112","volume":"79","author":"JJ Kozich","year":"2013","unstructured":"Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applenvironmicrobiol. 2013;79:5112\u201320.","journal-title":"Applenvironmicrobiol."},{"key":"1174_CR41","doi-asserted-by":"crossref","unstructured":"Zhang X, Li Xa SQ, Cao Q, Li C, Niu Q, et al. A curated 16S rRNA reference database for the classification of honeybee and bumblebee gut microbiota. Biodivers Sci. 2019;27.","DOI":"10.17520\/biods.2019021"},{"key":"1174_CR42","doi-asserted-by":"publisher","first-page":"2909","DOI":"10.1093\/bioinformatics\/btv269","volume":"31","author":"CP Zachary","year":"2015","unstructured":"Zachary CP, Brady SF. phylogeo: an R package for geographic analysis and visualization of microbiome data. Bioinformatics. 2015;31:2909\u201311.","journal-title":"Bioinformatics."},{"key":"1174_CR43","doi-asserted-by":"publisher","first-page":"927","DOI":"10.1111\/j.1654-1103.2003.tb02228.x","volume":"14","author":"P Dixon","year":"2003","unstructured":"Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci. 2003;14:927\u201330.","journal-title":"J Veg Sci"},{"key":"1174_CR44","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1002\/mas.21540","volume":"39","author":"LK Pino","year":"2020","unstructured":"Pino LK, Searle BC, Bollinger JG, Nunn B, MacLean B, MacCoss MJ. The Skyline ecosystem: informatics for quantitative mass spectrometry proteomics. Mass Spectrom Rev. 2020;39:229\u201344.","journal-title":"Mass Spectrom Rev"},{"key":"1174_CR45","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","volume":"37","author":"D Kim","year":"2019","unstructured":"Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37:907\u201315.","journal-title":"Nat Biotechnol"},{"key":"1174_CR46","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1038\/nbt.3122","volume":"33","author":"M Pertea","year":"2015","unstructured":"Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33:290\u20135.","journal-title":"Nat Biotechnol"},{"key":"1174_CR47","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.","journal-title":"Genome Biol"},{"key":"1174_CR48","doi-asserted-by":"publisher","first-page":"5593","DOI":"10.1073\/pnas.1419161111","volume":"111","author":"S Shen","year":"2014","unstructured":"Shen S, Park JW, Lu ZX, Lin L, Henry MD, Wu YN, et al. rMATS: robust and flexible detection of differential alternative splicing from replicate RNA-Seq data. Proc Natl Acad Sci U S A. 2014;111:5593\u2013601.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1174_CR49","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1038\/ng.3077","volume":"46","author":"A Wallberg","year":"2014","unstructured":"Wallberg A, Han F, Wellhagen G, Dahle B, Kawata M, Haddad N, et al. A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera. Nat Genet. 2014;46:1081\u20138.","journal-title":"Nat Genet"},{"key":"1174_CR50","doi-asserted-by":"publisher","first-page":"e2001861","DOI":"10.1371\/journal.pbio.2001861","volume":"15","author":"K Raymann","year":"2017","unstructured":"Raymann K, Shaffer Z, Moran NA. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol. 2017;15:e2001861.","journal-title":"PLoS Biol"},{"key":"1174_CR51","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1038\/s41396-019-0568-8","volume":"14","author":"L Kesnerova","year":"2020","unstructured":"Kesnerova L, Emery O, Troilo M, Liberti J, Erkosar B, Engel P. Gut microbiota structure differs between honeybees in winter and summer. ISME J. 2020;14:801\u201314.","journal-title":"ISME J"},{"key":"1174_CR52","doi-asserted-by":"publisher","first-page":"374","DOI":"10.1038\/nrmicro.2016.43","volume":"14","author":"WK Kwong","year":"2016","unstructured":"Kwong WK, Moran NA. Gut microbial communities of social bees. Nat Rev Microbiol. 2016;14:374\u201384.","journal-title":"Nat Rev Microbiol"},{"key":"1174_CR53","doi-asserted-by":"publisher","first-page":"13887","DOI":"10.1073\/pnas.1610856113","volume":"113","author":"JE Powell","year":"2016","unstructured":"Powell JE, Leonard SP, Kwong WK, Engel P, Moran NA. Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont. Proc Natl Acad Sci U S A. 2016;113:13887\u201392.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1174_CR54","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1016\/j.tim.2020.02.003","volume":"28","author":"K Ligthart","year":"2020","unstructured":"Ligthart K, Belzer C, de Vos WM, Tytgat HLP. Bridging bacteria and the gut: functional aspects of type IV pili. Trends Microbiol. 2020;28:340\u20138.","journal-title":"Trends Microbiol"},{"key":"1174_CR55","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1038\/ng.3507","volume":"48","author":"G Sveinbjornsson","year":"2016","unstructured":"Sveinbjornsson G, Albrechtsen A, Zink F, Gudjonsson SA, Oddson A, Masson G, et al. Weighting sequence variants based on their annotation increases power of whole-genome association studies. Nat Genet. 2016;48:314\u20137.","journal-title":"Nat Genet"},{"key":"1174_CR56","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.neulet.2004.02.004","volume":"359","author":"M Funada","year":"2004","unstructured":"Funada M, Yasuo S, Yoshimura T, Ebihara S, Sasagawa H, Kitagawa Y, et al. Characterization of the two distinct subtypes of metabotropic glutamate receptors from honeybee, Apis mellifera. Neurosci Lett. 2004;359:190\u20134.","journal-title":"Neurosci Lett"},{"key":"1174_CR57","doi-asserted-by":"publisher","first-page":"9313","DOI":"10.1074\/jbc.M310878200","volume":"279","author":"C Mitri","year":"2004","unstructured":"Mitri C, Parmentier ML, Pin JP, Bockaert J, Grau Y. Divergent evolution in metabotropic glutamate receptors. A new receptor activated by an endogenous ligand different from glutamate in insects. J Biol Chem. 2004;279:9313\u201320.","journal-title":"J Biol Chem"},{"key":"1174_CR58","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1146\/annurev.pharmtox.011008.145533","volume":"50","author":"CM Niswender","year":"2010","unstructured":"Niswender CM, Conn PJ. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol. 2010;50:295\u2013322.","journal-title":"Annu Rev Pharmacol Toxicol"},{"key":"1174_CR59","doi-asserted-by":"publisher","first-page":"16086","DOI":"10.1523\/JNEUROSCI.0714-14.2014","volume":"34","author":"D Raccuglia","year":"2014","unstructured":"Raccuglia D, Mueller U. Temporal integration of cholinergic and GABAergic inputs in isolated insect mushroom body neurons exposes pairing-specific signal processing. J Neurosci. 2014;34:16086\u201392.","journal-title":"J Neurosci"},{"key":"1174_CR60","doi-asserted-by":"publisher","first-page":"1718","DOI":"10.1111\/j.1460-9568.2012.08090.x","volume":"35","author":"AF Choudhary","year":"2012","unstructured":"Choudhary AF, Laycock I, Wright GA. Gamma-Aminobutyric acid receptor A-mediated inhibition in the honeybee\u02bcs antennal lobe is necessary for the formation of configural olfactory percepts. Eur J Neurosci. 2012;35:1718\u201324.","journal-title":"Eur J Neurosci"},{"key":"1174_CR61","doi-asserted-by":"publisher","first-page":"567","DOI":"10.1021\/acschemneuro.9b00599","volume":"11","author":"H Sakairi","year":"2020","unstructured":"Sakairi H, Kamikubo Y, Abe M, Ikeda K, Ichiki A, Tabata T, et al. G protein-coupled glutamate and GABA receptors form complexes and mutually modulate their signals. ACS Chem Neurosci. 2020;11:567\u201378.","journal-title":"ACS Chem Neurosci"},{"key":"1174_CR62","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1264\/jsme2.ME15019","volume":"30","author":"J Ludvigsen","year":"2015","unstructured":"Ludvigsen J, Rangberg A, Avershina E, Sekelja M, Kreibich C, Amdam G, et al. Shifts in the midgut\/pyloric microbiota composition within a honey bee apiary throughout a season. Microbes Environ. 2015;30:235\u201344.","journal-title":"Microbes Environ"},{"key":"1174_CR63","doi-asserted-by":"publisher","first-page":"291","DOI":"10.3390\/insects11050291","volume":"11","author":"VA Ricigliano","year":"2020","unstructured":"Ricigliano VA, Anderson KE. Probing the honey bee diet-microbiota-host axis using pollen restriction and organic acid feeding. Insects. 2020;11:291.","journal-title":"Insects."},{"key":"1174_CR64","doi-asserted-by":"publisher","first-page":"e00694","DOI":"10.1128\/mSphere.00694-20","volume":"5","author":"LM Bobay","year":"2020","unstructured":"Bobay LM, Wissel EF, Raymann K. Strain structure and dynamics revealed by targeted deep sequencing of the honey bee gut microbiome. Msphere. 2020;5:e00694\u201320.","journal-title":"Msphere."},{"key":"1174_CR65","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1038\/nature12480","volume":"500","author":"A Cotillard","year":"2013","unstructured":"Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N, Le Chatelier E, et al. Dietary intervention impact on gut microbial gene richness. Nature. 2013;500:585\u20138.","journal-title":"Nature."},{"key":"1174_CR66","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1038\/ismej.2012.146","volume":"7","author":"S Tims","year":"2013","unstructured":"Tims S, Derom C, Jonkers DM, Vlietinck R, Saris WH, Kleerebezem M, et al. Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 2013;7:707\u201317.","journal-title":"ISME J"},{"key":"1174_CR67","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1146\/annurev-genet-110711-155610","volume":"46","author":"RE Page Jr","year":"2012","unstructured":"Page RE Jr, Rueppell O, Amdam GV. Genetics of reproduction and regulation of honeybee (Apis mellifera L.) social behavior. Annu Rev Genet. 2012;46:97\u2013119.","journal-title":"Annu Rev Genet"},{"key":"1174_CR68","doi-asserted-by":"publisher","first-page":"eaaw3159","DOI":"10.1126\/scisignal.aaw3159","volume":"12","author":"T Yardeni","year":"2019","unstructured":"Yardeni T, Tanes CE, Bittinger K, Mattei LM, Schaefer PM, Singh LN, et al. Host mitochondria influence gut microbiome diversity: a role for ROS. Sci Signal. 2019;12:eaaw3159.","journal-title":"Sci Signal"},{"key":"1174_CR69","doi-asserted-by":"publisher","first-page":"1148","DOI":"10.1073\/pnas.1908600116","volume":"117","author":"NM Morella","year":"2020","unstructured":"Morella NM, Weng FC, Joubert PM, Metcalf CJE, Lindow S, Koskella B. Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection. Proc Natl Acad Sci U S A. 2020;117:1148\u201359.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1174_CR70","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1016\/j.celrep.2019.09.010","volume":"29","author":"AA Khan","year":"2019","unstructured":"Khan AA, Yurkovetskiy L, O\u2019Grady K, Pickard JM, de Pooter R, Antonopoulos DA, et al. Polymorphic immune mechanisms regulate commensal repertoire. Cell Rep. 2019;29:541\u201350 e4.","journal-title":"Cell Rep"},{"key":"1174_CR71","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1146\/annurev-micro-092412-155630","volume":"67","author":"E Kondorosi","year":"2013","unstructured":"Kondorosi E, Mergaert P, Kereszt A. A paradigm for endosymbiotic life: cell differentiation of Rhizobium bacteria provoked by host plant factors. Annu Rev Microbiol. 2013;67:611\u201328.","journal-title":"Annu Rev Microbiol"},{"key":"1174_CR72","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1038\/nrmicro957","volume":"2","author":"SV Nyholm","year":"2004","unstructured":"Nyholm SV, McFall-Ngai MJ. The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol. 2004;2:632\u201342.","journal-title":"Nat Rev Microbiol"},{"key":"1174_CR73","doi-asserted-by":"publisher","first-page":"552","DOI":"10.1016\/j.chom.2017.09.005","volume":"22","author":"N Tegtmeyer","year":"2017","unstructured":"Tegtmeyer N, Wessler S, Necchi V, Rohde M, Harrer A, Rau TT, et al. Helicobacter pylori employs a unique basolateral type IV secretion mechanism for CagA delivery. Cell Host Microbe. 2017;22:552\u201360 e5.","journal-title":"Cell Host Microbe"},{"key":"1174_CR74","doi-asserted-by":"publisher","first-page":"e13004","DOI":"10.1111\/cmi.13004","volume":"21","author":"A Wagner","year":"2019","unstructured":"Wagner A, Dehio C. Role of distinct type-IV-secretion systems and secreted effector sets in host adaptation by pathogenic Bartonella species. Cell Microbiol. 2019;21:e13004.","journal-title":"Cell Microbiol"},{"key":"1174_CR75","doi-asserted-by":"publisher","first-page":"1469","DOI":"10.1038\/ng.2007.38","volume":"39","author":"HL Saenz","year":"2007","unstructured":"Saenz HL, Engel P, Stoeckli MC, Lanz C, Raddatz G, Vayssier-Taussat M, et al. Genomic analysis of Bartonella identifies type IV secretion systems as host adaptability factors. Nat Genet. 2007;39:1469\u201376.","journal-title":"Nat Genet"},{"key":"1174_CR76","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1007\/s00335-014-9540-0","volume":"25","author":"A O'Connor","year":"2014","unstructured":"O'Connor A, Quizon PM, Albright JE, Lin FT, Bennett BJ. Responsiveness of cardiometabolic-related microbiota to diet is influenced by host genetics. Mamm Genome. 2014;25:583\u201399.","journal-title":"Mamm Genome"},{"key":"1174_CR77","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1038\/nature11234","volume":"486","author":"Human Microbiome Project C","year":"2012","unstructured":"Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207\u201314.","journal-title":"Nature."},{"key":"1174_CR78","doi-asserted-by":"publisher","first-page":"1558","DOI":"10.1101\/gr.194118.115","volume":"25","author":"E Org","year":"2015","unstructured":"Org E, Parks BW, Joo JW, Emert B, Schwartzman W, Kang EY, et al. Genetic and environmental control of host-gut microbiota interactions. Genome Res. 2015;25:1558\u201369.","journal-title":"Genome Res"},{"key":"1174_CR79","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1016\/j.chom.2018.06.007","volume":"24","author":"M Yassour","year":"2018","unstructured":"Yassour M, Jason E, Hogstrom LJ, Arthur TD, Tripathi S, Siljander H, et al. Strain-level analysis of mother-to-child bacterial transmission during the first few months of life. Cell Host Microbe. 2018;24:146\u201354 e4.","journal-title":"Cell Host Microbe"},{"key":"1174_CR80","doi-asserted-by":"publisher","first-page":"1206","DOI":"10.1111\/ejn.13929","volume":"47","author":"SA Quraishi","year":"2018","unstructured":"Quraishi SA, Paladini CA. Could GABA, with a side of glycine, control glutamate receptors? Eur J Neurosci. 2018;47:1206\u20137.","journal-title":"Eur J Neurosci"},{"key":"1174_CR81","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1016\/0742-8413(89)90065-0","volume":"92","author":"E Fuchs","year":"1989","unstructured":"Fuchs E, Dustmann JH, Stadler H, Sch\u00fcrmann FW. Neuroactive compounds in the brain of the honeybee during imaginal life. Comp Biochem Physiol C. 1989;92:337\u201342.","journal-title":"Comp Biochem Physiol C"},{"key":"1174_CR82","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1002\/(SICI)1097-0029(19990501)45:3<174::AID-JEMT5>3.0.CO;2-U","volume":"45","author":"G Bicker","year":"1999","unstructured":"Bicker G. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech. 1999;45:174\u201383.","journal-title":"Microsc Res Tech"},{"key":"1174_CR83","doi-asserted-by":"publisher","first-page":"1600","DOI":"10.1016\/j.cell.2019.05.004","volume":"177","author":"G Sharon","year":"2019","unstructured":"Sharon G, Cruz NJ, Kang DW, Gandal MJ, Wang B, Kim YM, et al. Human gut microbiota from autism spectrum disorder promote behavioral symptoms in mice. Cell. 2019;177:1600\u201318 e17.","journal-title":"Cell."},{"key":"1174_CR84","doi-asserted-by":"publisher","first-page":"9653","DOI":"10.1073\/pnas.1708127114","volume":"114","author":"HY Shpigler","year":"2017","unstructured":"Shpigler HY, Saul MC, Corona F, Block L, Cash Ahmed A, Zhao SD, et al. Deep evolutionary conservation of autism-related genes. Proc Natl Acad Sci U S A. 2017;114:9653\u20138.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1174_CR85","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1016\/j.cois.2020.01.004","volume":"39","author":"J Liberti","year":"2020","unstructured":"Liberti J, Engel P. The gut microbiota-brain axis of insects. Curr Opin Insect Sci. 2020;39:6\u201313.","journal-title":"Curr Opin Insect Sci"},{"key":"1174_CR86","doi-asserted-by":"publisher","first-page":"362","DOI":"10.1126\/science.1143046","volume":"317","author":"HR Mattila","year":"2007","unstructured":"Mattila HR, Seeley TD. Genetic diversity in honey bee colonies enhances productivity and fitness. Science. 2007;317:362\u20134.","journal-title":"Science."},{"key":"1174_CR87","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1051\/apido:19940204","volume":"25","author":"S Fuchs","year":"1994","unstructured":"Fuchs S, Schade V. Lower performance in honeybee colonies of uniform paternity. Apidologie. 1994;25:155\u201368.","journal-title":"Apidologie."},{"key":"1174_CR88","first-page":"1","volume":"46","author":"BJ Eckholm","year":"2014","unstructured":"Eckholm BJ, Huang MH, Anderson KE, Mott BM, Degrandi-Hoffman G. Honey bee (Apis mellifera) intracolonial genetic diversity influences worker nutritional status. Apidologie. 2014;46:1\u201314.","journal-title":"Apidologie."},{"key":"1174_CR89","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1146\/annurev.ento.010908.164537","volume":"55","author":"MV Srinivasan","year":"2010","unstructured":"Srinivasan MV. Honey bees as a model for vision, perception, and cognition. Annu Rev Entomol. 2010;55:267\u201384.","journal-title":"Annu Rev Entomol"},{"key":"1174_CR90","doi-asserted-by":"publisher","first-page":"348","DOI":"10.3390\/insects10100348","volume":"10","author":"H Kohno","year":"2019","unstructured":"Kohno H, Kubo T. Genetics in the honey bee: achievements and prospects toward the functional analysis of molecular and neural mechanisms underlying social behaviors. Insects. 2019;10:348.","journal-title":"Insects."}],"container-title":["Microbiome"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40168-021-01174-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s40168-021-01174-y\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40168-021-01174-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,8]],"date-time":"2023-02-08T23:04:16Z","timestamp":1675897456000},"score":1,"resource":{"primary":{"URL":"https:\/\/microbiomejournal.biomedcentral.com\/articles\/10.1186\/s40168-021-01174-y"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,17]]},"references-count":90,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["1174"],"URL":"https:\/\/doi.org\/10.1186\/s40168-021-01174-y","relation":{},"ISSN":["2049-2618"],"issn-type":[{"value":"2049-2618","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,17]]},"assertion":[{"value":"9 June 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 September 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 November 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"225"}}