{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T14:28:56Z","timestamp":1785421736423,"version":"3.56.0"},"reference-count":31,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2026,7,4]],"date-time":"2026-07-04T00:00:00Z","timestamp":1783123200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32360141"],"award-info":[{"award-number":["32360141"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["32360141"],"award-info":[{"award-number":["32360141"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100011812","name":"Student Innovative Ability Training Program Project of the College of Animal Science and Technology, Yunnan Agricultural University","doi-asserted-by":"publisher","award":["A3012025077"],"award-info":[{"award-number":["A3012025077"]}],"id":[{"id":"10.13039\/501100011812","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Earmarked Fund for China Agriculture Research System of MOF and MARA","award":["CARS-44-KXJ13"],"award-info":[{"award-number":["CARS-44-KXJ13"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Bumblebees are dominant pollinators threatened by environmental antibiotic residues. This study investigated sublethal chloramphenicol (12 and 120 \u03bcg\/L) effects on Bombus terrestris after 15 days\u2019 exposure. The results showed that chloramphenicol exposure had no significant effect on the survival rate and cumulative food intake of bumblebees, confirming the sublethal property of the tested concentrations. However, chloramphenicol significantly dysregulated the expression of genes related to learning\u2013memory (DopR2, Oamb, NMDA), immunity (abaecin, defensin) and detoxification (cyp9Q6) in bumblebees. High-dose chloramphenicol significantly increased carboxylesterase activity and reduced malondialdehyde content, while superoxide dismutase activity remained unchanged. In addition, chloramphenicol exposure significantly reshaped the gut microbiota structure of bumblebees, reduced the abundance of core beneficial symbiotic bacteria, and increased the proportion of drug-resistant bacteria. Our findings indicate that sublethal concentrations of chloramphenicol can impair bumblebee health through multiple pathways, including regulating gene expression, altering antioxidant enzyme activity and disrupting gut microbiota homeostasis. This study provides multi-dimensional toxicological data and a scientific basis for the ecological risk assessment of agricultural antibiotic residues to pollinator insects.<\/jats:p>","DOI":"10.3390\/ijms27136004","type":"journal-article","created":{"date-parts":[[2026,7,6]],"date-time":"2026-07-06T13:43:14Z","timestamp":1783345394000},"page":"6004","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Sublethal Concentration of Chloramphenicol Threatens the Health of Bombus terrestris by Regulating Gene Expression, Altering Enzyme Activity and Disrupting Gut Microbiota"],"prefix":"10.3390","volume":"27","author":[{"given":"Zhu","family":"Qin","sequence":"first","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuai","family":"Guo","sequence":"additional","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuang","family":"Wang","sequence":"additional","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xi","family":"Xu","sequence":"additional","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haijun","family":"Bai","sequence":"additional","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bian","family":"Zhao","sequence":"additional","affiliation":[{"name":"Sericulture and Apiculture Research Institute, Yunnan Academy of Agricultural Sciences, Mengzi 661100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheng","family":"Liang","sequence":"additional","affiliation":[{"name":"Sericulture and Apiculture Research Institute, Yunnan Academy of Agricultural Sciences, Mengzi 661100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kun","family":"Dong","sequence":"additional","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xueyang","family":"Gong","sequence":"additional","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yakai","family":"Tian","sequence":"additional","affiliation":[{"name":"Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"108068","DOI":"10.1016\/j.ecolecon.2023.108068","article-title":"Impacts of degraded pollination ecosystem services on global food security and nutrition","volume":"217","author":"Uwingabire","year":"2024","journal-title":"Ecol. Econ."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.tree.2010.01.007","article-title":"Global pollinator declines: Trends, impacts and drivers","volume":"25","author":"Potts","year":"2010","journal-title":"Trends Ecol. Evol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Bie, M., Song, K., Dong, H., Zhao, W., Lin, H., Shi, D., and Liu, D. (2025). Advancing sustainable agriculture through bumblebee pollination: Bibliometric insights and future directions. Sustainability, 17.","DOI":"10.3390\/su17052177"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.cois.2017.06.001","article-title":"Bumble bee ecophysiology: Integrating the changing environment and the organism","volume":"22","author":"Woodard","year":"2017","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"231","DOI":"10.15386\/mpr-1742","article-title":"Antibiotics in the environment: Causes and consequences","volume":"93","author":"Polianciuc","year":"2020","journal-title":"Med. Pharm. Rep."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Manyi-Loh, C., Mamphweli, S., Meyer, E., and Okoh, A. (2018). Antibiotic use in agriculture and its consequential resistance in environmental sources: Potential public health implications. Molecules, 23.","DOI":"10.3390\/molecules23040795"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1093\/jaoac\/91.5.1103","article-title":"Determination of Chloramphenicol Residues in Bee Pollen by Liquid Chromatography\/TandemMass Spectrometry","volume":"91","author":"Fujita","year":"2008","journal-title":"J. AOAC Int."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"340841","DOI":"10.1016\/j.aca.2023.340841","article-title":"Ultrasensitive detection of ineradicable and harmful antibiotic chloramphenicol residue in soil, water, and food samples","volume":"1243","author":"Karikalan","year":"2023","journal-title":"Anal. Chim. Acta"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1007\/s11101-019-09642-y","article-title":"For antagonists and mutualists: The paradox of insect toxic secondary metabolites in nectar and pollen","volume":"19","author":"Stevenson","year":"2020","journal-title":"Phytochem. Rev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1098\/rspb.2007.1652","article-title":"The correlation of learning speed and natural foraging success in bumble-bees","volume":"275","author":"Raine","year":"2008","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Xu, J., Strange, J.P., Welker, D.L., and James, R.R. (2013). Detoxification and stress response genes expressed in a western North American bumble bee, Bombus huntii (Hymenoptera: Apidae). BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-874"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"16003","DOI":"10.1038\/npjbiofilms.2016.3","article-title":"The gut microbiota: A major player in the toxicity of environmental pollutants?","volume":"2","author":"Claus","year":"2016","journal-title":"npj Biofilms Microbiomes"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Aresta, A.M., De Vietro, N., Mancini, G., and Zambonin, C. (2026). Chloramphenicol residue analysis in food and environmental matrices: Regulatory framework and advances in trace-level determination. Molecules, 31.","DOI":"10.3390\/molecules31091440"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Yu, T., and Zeng, F. (2024). Chloramphenicol interferes with 50s ribosomal subunit maturation via direct and indirect mechanisms. Biomolecules, 14.","DOI":"10.3390\/biom14101225"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1087","DOI":"10.1038\/s41893-025-01603-y","article-title":"Impacts of antibiotic use, air pollution and climate on managed honeybees in Canada","volume":"8","author":"Daisley","year":"2025","journal-title":"Nat. Sustain."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Raymann, K., Shaffer, Z., and Moran, N.A. (2017). Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol., 15.","DOI":"10.1371\/journal.pbio.2001861"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"139628","DOI":"10.1016\/j.jhazmat.2025.139628","article-title":"Larval antibiotic exposure causes persistent impacts on honeybees across life stages via metabolic succession","volume":"497","author":"Shi","year":"2025","journal-title":"J. Hazard. Mater."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1134\/S1061934818040044","article-title":"Methods of determination of antibiotic residues in honey","volume":"73","author":"Ratajac","year":"2018","journal-title":"J. Anal. Chem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1929","DOI":"10.1007\/s10311-022-01416-x","article-title":"Occurrence, toxicity and adsorptive removal of the chloramphenicol antibiotic in water: A review","volume":"20","author":"Nguyen","year":"2022","journal-title":"Environ. Chem. Lett."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1016\/j.envpol.2017.08.051","article-title":"Transfer of antibiotics from wastewater or animal manure to soil and edible crops","volume":"231","author":"Pan","year":"2017","journal-title":"Environ. Pollut."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1007\/s13592-019-00718-4","article-title":"Antibiotic treatment impairs protein digestion in the honeybee, Apis mellifera","volume":"51","author":"Stutzer","year":"2020","journal-title":"Apidologie"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.15666\/aeer\/1801_13171327","article-title":"Differential roles for dopamine D1-like and D2-like receptors in learning and behavior of honeybee and other insects","volume":"18","author":"Raza","year":"2020","journal-title":"Appl. Ecol. Environ. Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Bazzari, A.H., and Parri, H.R. (2019). Neuromodulators and long-term synaptic plasticity in learning and memory: A steered-glutamatergic perspective. Brain Sci., 9.","DOI":"10.3390\/brainsci9110300"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"101457","DOI":"10.1016\/j.cois.2025.101457","article-title":"The role of insulin and octopamine in regulating energy homeostasis and locomotion in insects","volume":"73","author":"Bisen","year":"2026","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_25","first-page":"457","article-title":"Changes in the expression of antimicrobial peptide genes in honey bees (Apis mellifera) under the influence of various pathogens","volume":"66","author":"Pluta","year":"2020","journal-title":"Ann. Parasitol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e2205850119","DOI":"10.1073\/pnas.2205850119","article-title":"Phylogenomic and functional characterization of an evolutionary conserved cytochrome P450-based insecticide detoxification mechanism in bees","volume":"119","author":"Haas","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"272","DOI":"10.3390\/physiologia3020019","article-title":"Response of Superoxide Dismutase (SOD) to Homogeneous and Heterogeneous Food Sources in Bumblebees (Bombus terrestris) and Honeybees (Apis mellifera)","volume":"3","author":"Ludewig","year":"2023","journal-title":"Physiologia"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"28322","DOI":"10.1038\/s41598-025-14089-7","article-title":"Redox metabolic disruptions in the honey bee brain following acute exposure to the pyrethroid deltamethrin","volume":"15","author":"Mackei","year":"2025","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1016\/j.ecoenv.2011.03.002","article-title":"Chronic accumulation of cadmium and its effects on antioxidant enzymes and malondialdehyde in Oxya chinensis (Orthoptera: Acridoidea)","volume":"74","author":"Zhang","year":"2011","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Khan, S.A., Kojour, M.A.M., and Han, Y.S. (2023). Recent trends in insect gut immunity. Front. Immunol., 14.","DOI":"10.3389\/fimmu.2023.1272143"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1128\/AAC.00870-08","article-title":"Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition","volume":"53","author":"Siibak","year":"2009","journal-title":"Antimicrob. Agents Chemother."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/13\/6004\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,6]],"date-time":"2026-07-06T13:49:31Z","timestamp":1783345771000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/13\/6004"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,4]]},"references-count":31,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2026,7]]}},"alternative-id":["ijms27136004"],"URL":"https:\/\/doi.org\/10.3390\/ijms27136004","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,4]]}}}