{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T04:12:16Z","timestamp":1773115936165,"version":"3.50.1"},"reference-count":98,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,12,1]],"date-time":"2022-12-01T00:00:00Z","timestamp":1669852800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"German Research Foundation","doi-asserted-by":"publisher","award":["(KO 5604\/1\u20131"],"award-info":[{"award-number":["(KO 5604\/1\u20131"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004199","name":"Okinawa Institute of Science and Technology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004199","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000923","name":"Australian Research Council","doi-asserted-by":"publisher","award":["FT160100178"],"award-info":[{"award-number":["FT160100178"]}],"id":[{"id":"10.13039\/501100000923","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Microbiomes can enhance the health, fitness and even evolutionary potential of their hosts. Many organisms propagate favorable microbiomes fully or partially <jats:italic>via<\/jats:italic> vertical transmission. In the long term, such co-propagation can lead to the evolution of specialized microbiomes and functional interdependencies with the host. However, microbiomes are vulnerable to environmental stressors, particularly anthropogenic disturbance such as antibiotics, resulting in dysbiosis. In cases where microbiome transmission occurs, a disrupted microbiome may then become a contagious pathology causing harm to the host across generations. We tested this hypothesis using the specialized socially transmitted gut microbiome of honey bees as a model system. By experimentally passaging tetracycline-treated microbiomes across worker \u2018generations\u2019 we found that an environmentally acquired dysbiotic phenotype is heritable. As expected, the antibiotic treatment disrupted the microbiome, eliminating several common and functionally important taxa and strains. When transmitted, the dysbiotic microbiome harmed the host in subsequent generations. Particularly, na\u00efve bees receiving antibiotic-altered microbiomes died at higher rates when challenged with further antibiotic stress. Bees with inherited dysbiotic microbiomes showed alterations in gene expression linked to metabolism and immunity, among other pathways, suggesting effects on host physiology. These results indicate that there is a possibility that sublethal exposure to chemical stressors, such as antibiotics, may cause long-lasting changes to functional host-microbiome relationships, possibly weakening the host\u2019s progeny in the face of future ecological challenges. Future studies under natural conditions would be important to examine the extent to which negative microbiome-mediated phenotypes could indeed be heritable and what role this may play in the ongoing loss of biodiversity.<\/jats:p>","DOI":"10.3389\/fmicb.2022.1030771","type":"journal-article","created":{"date-parts":[[2022,12,1]],"date-time":"2022-12-01T17:57:11Z","timestamp":1669917431000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":10,"title":["Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations"],"prefix":"10.3389","volume":"13","author":[{"given":"Vienna","family":"Kowallik","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ashutosh","family":"Das","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexander S.","family":"Mikheyev","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2022,12,1]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1016\/j.tree.2016.06.008","article-title":"Do vertebrate gut metagenomes confer rapid ecological adaptation?","volume":"31","author":"Alberdi","year":"2016","journal-title":"Trends Ecol. 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Insect Physiol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1021\/acs.estlett.8b00597","article-title":"Perfluorobutanesulfonate exposure causes durable and transgenerational Dysbiosis of gut microbiota in marine Medaka","volume":"5","author":"Chen","year":"2018","journal-title":"Environ. Sci. Technol. Lett."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"705","DOI":"10.1016\/j.cell.2014.05.052","article-title":"Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences","volume":"158","author":"Cox","year":"2014","journal-title":"Cells"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"717990","DOI":"10.3389\/fmicb.2021.717990","article-title":"Resistance and vulnerability of honeybee (Apis mellifera) gut bacteria to commonly used pesticides","volume":"12","author":"Cuesta-Mat\u00e9","year":"2021","journal-title":"Front. 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Microbiol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"446","DOI":"10.1038\/s41467-019-08303-0","article-title":"Genomic diversity landscape of the honey bee gut microbiota","volume":"10","author":"Ellegaard","year":"2019","journal-title":"Nat. Commun."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"2576","DOI":"10.1111\/mec.14058","article-title":"Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera)","volume":"26","author":"Emery","year":"2017","journal-title":"Mol. Ecol."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3896\/IBRA.1.52.4.07","article-title":"Standard methods for research on Apis mellifera gut symbionts","volume":"52","author":"Engel","year":"2013","journal-title":"J. Apic. Res."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"e02164","DOI":"10.1128\/mBio.02164-15","article-title":"The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions","volume":"7","author":"Engel","year":"2016","journal-title":"MBio"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1111\/1574-6976.12025","article-title":"The gut microbiota of insects \u2013 diversity in structure and function","volume":"37","author":"Engel","year":"2013","journal-title":"FEMS Microbiol. Rev."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1111\/j.1365-2583.2006.00682.x","article-title":"Immune pathways and defence mechanisms in honey bees Apis mellifera","volume":"15","author":"Evans","year":"2006","journal-title":"Insect Mol. Biol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1093\/bioinformatics\/btl567","article-title":"Using GOstats to test gene lists for GO term association","volume":"23","author":"Falcon","year":"2007","journal-title":"Bioinformatics"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"e77263","DOI":"10.1371\/journal.pone.0077263","article-title":"Non-specific dsRNA-mediated antiviral response in the honey bee","volume":"8","author":"Flenniken","year":"2013","journal-title":"PLoS One"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1038\/nrgastro.2012.156","article-title":"The role of the gut microbiota in nutrition and health","volume":"9","author":"Flint","year":"2012","journal-title":"Nat. Rev. Gastroenterol. 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Microbiol."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1038\/ni.2608","article-title":"Control of pathogens and pathobionts by the gut microbiota","volume":"14","author":"Kamada","year":"2013","journal-title":"Nat. Immunol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1734","DOI":"10.12688\/f1000research.16680.1","article-title":"Ranacapa: an R package and shiny web app to explore environmental DNA data with exploratory statistics and interactive visualizations","volume":"7","author":"Kandlikar","year":"2018","journal-title":"F1000Res"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"e2003467","DOI":"10.1371\/journal.pbio.2003467","article-title":"Disentangling metabolic functions of bacteria in the honey bee gut","volume":"15","author":"Ke\u0161nerov\u00e1","year":"2017","journal-title":"PLoS Biol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"8618","DOI":"10.1073\/pnas.1200231109","article-title":"Symbiont-mediated insecticide resistance","volume":"109","author":"Kikuchi","year":"2012","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"e1","DOI":"10.1093\/nar\/gks808","article-title":"Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies","volume":"41","author":"Klindworth","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"2028","DOI":"10.1111\/mec.12209","article-title":"Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees","volume":"22","author":"Koch","year":"2013","journal-title":"Mol. Ecol."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"e02966","DOI":"10.1128\/mBio.02966-21","article-title":"Honey bee larval and adult microbiome life stages are effectively decoupled with vertical transmission overcoming early life perturbations","volume":"12","author":"Kowallik","year":"2021","journal-title":"MBio"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"180","DOI":"10.3390\/microorganisms7060180","article-title":"Antibiotic pollution in the environment: from microbial ecology to public policy","volume":"7","author":"Kraemer","year":"2019","journal-title":"Microorganisms."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"e1600513","DOI":"10.1126\/sciadv.1600513","article-title":"Dynamic microbiome evolution in social bees","volume":"3","author":"Kwong","year":"2017","journal-title":"Sci. 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Ecol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1080\/02652030500469048","article-title":"Tetracycline residues in honey after hive treatment","volume":"23","author":"Martel","year":"2006","journal-title":"Food Additives Contaminants"},{"key":"ref57","doi-asserted-by":"publisher","first-page":"e61217","DOI":"10.1371\/journal.pone.0061217","article-title":"Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data","volume":"8","author":"McMurdie","year":"2013","journal-title":"PLoS One"},{"key":"ref58","doi-asserted-by":"publisher","first-page":"e1003531","DOI":"10.1371\/journal.pcbi.1003531","article-title":"Waste not, want not: why rarefying microbiome data is inadmissible","volume":"10","author":"McMurdie","year":"2014","journal-title":"PLoS Comput. Biol."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"4212","DOI":"10.1172\/JCI72333","article-title":"Antibiotics and the gut microbiota","volume":"124","author":"Modi","year":"2014","journal-title":"J. Clin. Invest."},{"key":"ref60","doi-asserted-by":"publisher","DOI":"10.1128\/mSystems.00268-20","article-title":"Impact of glyphosate on the honey bee gut microbiota: effects of intensity duration, and timing of exposure","volume":"5","author":"Motta","year":"2020","journal-title":"mSystems."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1186\/s42523-022-00165-0","article-title":"Glyphosate induces immune dysregulation in honey bees","volume":"4","author":"Motta","year":"2022","journal-title":"Animal Microbiome."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"1681","DOI":"10.1016\/j.celrep.2015.02.034","article-title":"Tetracyclines disturb mitochondrial function across eukaryotic models: a call for caution in biomedical research","volume":"10","author":"Moullan","year":"2015","journal-title":"Cell Rep."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"2055","DOI":"10.1111\/1365-2435.13493","article-title":"Microbial rescue effects: how microbiomes can save hosts from extinction","volume":"34","author":"Mueller","year":"2020","journal-title":"Funct. 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Microbiol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"1197","DOI":"10.1158\/0008-5472.CAN-14-2732","article-title":"Dietary microbes modulate transgenerational cancer risk","volume":"75","author":"Poutahidis","year":"2015","journal-title":"Cancer Res."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"e00103","DOI":"10.1128\/Spectrum.00103-21","article-title":"Field-realistic Tylosin exposure impacts honey bee microbiota and pathogen susceptibility, which is ameliorated by native gut probiotics","author":"Powell","year":"2021","journal-title":"Microbiol. Spectr."},{"key":"ref71","doi-asserted-by":"publisher","first-page":"7378","DOI":"10.1128\/AEM.01861-14","article-title":"Routes of acquisition of the gut microbiota of Apis mellifera","author":"Powell","year":"2014","journal-title":"Appl. Environ. 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Rev. Immunol."},{"key":"ref80","doi-asserted-by":"publisher","first-page":"3820","DOI":"10.1038\/s41598-019-40347-6","article-title":"Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure","volume":"9","author":"Rubanov","year":"2019","journal-title":"Sci. Rep."},{"key":"ref81","doi-asserted-by":"publisher","first-page":"20","DOI":"10.4066\/2529-8046.100025","article-title":"Assessment of ecological risks of agrochemicals requires a new framework","volume":"1","author":"S\u00e1nchez-Bayo","year":"2017","journal-title":"Environ. Risk Assess. Remediation."},{"key":"ref82","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1038\/s41564-017-0075-5","article-title":"Intergenerational transfer of antibiotic-perturbed microbiota enhances colitis in susceptible mice","volume":"3","author":"Schulfer","year":"2018","journal-title":"Nat. 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Genet."},{"key":"ref84","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1038\/nature16504","article-title":"Diet-induced extinctions in the gut microbiota compound over generations","volume":"529","author":"Sonnenburg","year":"2016","journal-title":"Nature"},{"key":"ref85","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1186\/s40168-022-01268-1","article-title":"Geographical resistome profiling in the honeybee microbiome reveals resistance gene transfer conferred by mobilizable plasmids","volume":"10","author":"Sun","year":"2022","journal-title":"Microbiome."},{"key":"ref86","doi-asserted-by":"publisher","first-page":"e21800","DOI":"10.1371\/journal.pone.0021800","article-title":"REVIGO summarizes and visualizes long lists of gene ontology terms","volume":"6","author":"Supek","year":"2011","journal-title":"PLoS One"},{"key":"ref87","doi-asserted-by":"publisher","first-page":"e00377","DOI":"10.1128\/mBio.00377-12","article-title":"Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees","volume":"3","author":"Tian","year":"2012","journal-title":"MBio"},{"key":"ref88","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1038\/nature11552","article-title":"Functional interactions between the gut microbiota and host metabolism","volume":"489","author":"Tremaroli","year":"2012","journal-title":"Nature"},{"key":"ref89","doi-asserted-by":"publisher","first-page":"1027","DOI":"10.1038\/nature05414","article-title":"An obesity-associated gut microbiome with increased capacity for energy harvest","volume":"444","author":"Turnbaugh","year":"2006","journal-title":"Nature"},{"key":"ref90","doi-asserted-by":"publisher","first-page":"213.e7","DOI":"10.1016\/j.chom.2020.01.009","article-title":"Changes in microbiome confer multigenerational host resistance after sub-toxic pesticide exposure","volume":"27","author":"Wang","year":"2020","journal-title":"Cell Host Microbe"},{"key":"ref91","doi-asserted-by":"publisher","first-page":"5261","DOI":"10.1128\/AEM.00062-07","article-title":"Na\u00efve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy","volume":"73","author":"Wang","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref92","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1038\/nrmicro2536","article-title":"Shifting the balance: antibiotic effects on host\u2013microbiota mutualism","volume":"9","author":"Willing","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"ref93","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1186\/s40168-021-01174-y","article-title":"Honey bee genetics shape the strain-level structure of gut microbiota in social transmission","volume":"9","author":"Wu","year":"2021","journal-title":"Microbiome"},{"key":"ref94","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1186\/s12864-020-6665-2","article-title":"The effect of antibiotics on the gut microbiome: a metagenomics analysis of microbial shift and gut antibiotic resistance in antibiotic treated mice","volume":"21","author":"Xu","year":"2020","journal-title":"BMC Genomics"},{"key":"ref95","doi-asserted-by":"publisher","first-page":"D643","DOI":"10.1093\/nar\/gkt1209","article-title":"The SILVA and \u201call-species living tree project (LTP)\u201d taxonomic frameworks","volume":"42","author":"Yilmaz","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref96","doi-asserted-by":"publisher","first-page":"4078","DOI":"10.1002\/1873-3468.13278","article-title":"The gut microbiome participates in transgenerational inheritance of low-temperature responses in Drosophila melanogaster","volume":"592","author":"Zare","year":"2018","journal-title":"FEBS Lett."},{"key":"ref97","doi-asserted-by":"publisher","first-page":"24712","DOI":"10.1073\/pnas.1915307116","article-title":"Obligate bacterial endosymbionts limit thermal tolerance of insect host species","volume":"116","author":"Zhang","year":"2019","journal-title":"PNAS"},{"key":"ref98","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1038\/s41684-018-0173-x","article-title":"Honey bees as models for gut microbiota research","volume":"47","author":"Zheng","year":"2018","journal-title":"Lab Anim."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.1030771\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,1]],"date-time":"2022-12-01T17:57:16Z","timestamp":1669917436000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.1030771\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,1]]},"references-count":98,"alternative-id":["10.3389\/fmicb.2022.1030771"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2022.1030771","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,1]]},"article-number":"1030771"}}