Gut Microbiota Dynamics and Phenotypic Changes Induced by Tetracycline in Drosophila melanogaster
Keywords:
Tetracycline, gut microbiota, phenotypic profile, Drosophila melanogaster
Abstract
Gut microbiota plays a crucial role in both physiological and pathological processes in humans and animals. Antibiotics, designed to combat bacterial infections, can induce alterations in the composition and abundance of the gut microbiota over prolonged exposure. This study addresses the limited understanding of the connections between gut microbiota and phenotypic profiles of metazoan species. We investigated the impact of early-life exposure to tetracycline in wild-type D. melanogaster, which were fed a standard diet, comparing them to a control group not exposed to tetracycline. The primary objective was to examine the consequences of early-life tetracycline exposure on gut microbiota and its implications for phenotypic profiles, including survival, locomotor activity, and reproduction in adult flies. Results revealed a significant reduction in lactic acid bacteria in adult flies exposed to tetracycline. However, tetracycline exhibited no interference with fly development, allowing them to maintain a normal lifespan. In adult flies, tetracycline significantly decreased the lifespan on day 35 at a concentration of 1000 µg/mL and reduced locomotion on day 27 at concentrations of 10 µg/mL and 1000 µg/mL. Remarkably, tetracycline did not impact the reproductive capabilities of the flies. This study demonstrates that while tetracycline led to a decline in lactic acid bacteria, locomotion, and lifespan in adult flies, it did not disrupt their development or reproductive processes.
References
Adembri, C., Novelli, A., & Nobili, S. (2020). Some Suggestions from PK/PD Principles to Contain Resistance in the Clinical Setting-Focus on ICU Patients and Gram-Negative Strains. Antibiotics (Basel), 9(10). https://doi.org/10.3390/antibiotics9100676
Ali, Y. O., Escala, W., Ruan, K., & Zhai, R. G. (2011). Assaying locomotor, learning, and memory deficits in Drosophila models of neurodegeneration. J Vis Exp(49). https://doi.org/10.3791/2504
Ashburner, M., & Roote, J. (2007). Maintenance of a Drosophila Laboratory: General Procedures. Cold Spring Harbor Protocols, 2007(3), pdb.ip35. https://doi.org/10.1101/pdb.ip35
Broderick, N. A., Buchon, N., & Lemaitre, B. (2014). Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. mBio, 5(3), e01117-01114. https://doi.org/10.1128/mBio.01117-14
Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S., & Lemaitre, B. (2009). Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe, 5(2), 200-211. https://doi.org/10.1016/j.chom.2009.01.003
Chao, H., Sun, M., Ye, M., Zheng, X., & Hu, F. (2020). World within world: Intestinal bacteria combining physiological parameters to investigate the response of Metaphire guillelmi to tetracycline stress. Environ Pollut, 261, 114174. https://doi.org/10.1016/j.envpol.2020.114174
Charroux, B., & Royet, J. (2012). Gut-microbiota interactions in non-mammals: what can we learn from Drosophila? Semin Immunol, 24(1), 17-24. https://doi.org/10.1016/j.smim.2011.11.003
Cheng, L., Baonza, A., & Grifoni, D. (2018). Drosophila Models of Human Disease. Biomed Res Int, 2018, 7214974. https://doi.org/10.1155/2018/7214974
Chopra, I., & Roberts, M. (2001). Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev, 65(2), 232-260 ; second page, table of contents. https://doi.org/10.1128/MMBR.65.2.232-260.2001
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O'Connor, E. M., Cusack, S., Harris, H. M., Coakley, M., Lakshminarayanan, B., O'Sullivan, O., Fitzgerald, G. F., Deane, J., O'Connor, M., Harnedy, N., O'Connor, K., O'Mahony, D., van Sinderen, D., Wallace, M., Brennan, L., . . . O'Toole, P. W. (2012). Gut microbiota composition correlates with diet and health in the elderly. Nature, 488(7410), 178-184. https://doi.org/10.1038/nature11319
Clark, R. I., Salazar, A., Yamada, R., Fitz-Gibbon, S., Morselli, M., Alcaraz, J., Rana, A., Rera, M., Pellegrini, M., Ja, W. W., & Walker, D. W. (2015). Distinct Shifts in Microbiota Composition during Drosophila Aging Impair Intestinal Function and Drive Mortality. Cell Rep, 12(10), 1656-1667. https://doi.org/10.1016/j.celrep.2015.08.004
Clark, R. I., & Walker, D. W. (2018). Role of gut microbiota in aging-related health decline: insights from invertebrate models. Cell Mol Life Sci, 75(1), 93-101. https://doi.org/10.1007/s00018-017-2671-1
de Man, J. C., Rogosa, M. and Sharpe, M.E. (1960). A Medium for the Cultivation of Lactobacilli. Journal of Applied Bacteriology, 23, 130-135. https://doi.org/https://doi.org/10.1111/j.1365-2672.1960.tb00188.x
de Vries, L. E., Valles, Y., Agerso, Y., Vaishampayan, P. A., Garcia-Montaner, A., Kuehl, J. V., Christensen, H., Barlow, M., & Francino, M. P. (2011). The gut as reservoir of antibiotic resistance: microbial diversity of tetracycline resistance in mother and infant. PLoS One, 6(6), e21644. https://doi.org/10.1371/journal.pone.0021644
di Cerbo, A., Pezzuto, F., Guidetti, G., Canello, S., & Corsi, L. (2019). Tetracyclines: Insights and Updates of their Use in Human and Animal Pathology and their Potential Toxicity. The Open Biochemistry Journal, 13(1), 1-12. https://doi.org/10.2174/1874091x01913010001
Enabulele, J. E., Chukwumah, N. M., & Enabulele, O. (2020). Tetracycline use in children and knowledge of its oral implications among nursing mothers. Pediatric Dental Journal, 30(3), 224-230. https://doi.org/10.1016/j.pdj.2020.08.003
Fan, Y., & Pedersen, O. (2021). Gut microbiota in human metabolic health and disease. Nat Rev Microbiol, 19(1), 55-71. https://doi.org/10.1038/s41579-020-0433-9
Gebrayel, P. N., C. Al Khodor, S. Bilinski, J. Caselli, E. Comelli, E. M. Egert, M. Giaroni, C. Karpinski, T. M. Loniewski, I. Mulak, A. Reygner, J. Samczuk, P. Serino, M. Sikora, M. Terranegra, A. Ufnal, M. Villeger, R. Pichon, C. Konturek, P. Edeas, M. (2022). Microbiota medicine: towards clinical revolution. J Transl Med, 20(1), 111. https://doi.org/10.1186/s12967-022-03296-9
Gilbert, J. A., Blaser, M. J., Caporaso, J. G., Jansson, J. K., Lynch, S. V., & Knight, R. (2018). Current understanding of the human microbiome. Nat Med, 24(4), 392-400. https://doi.org/10.1038/nm.4517
Gökçe Üstündağ, K. B., Ender Büyükgüzel. (2020). Penicillin Impact on Survivorship, Development, and Adult Longevity of Drosophila melanogaster (Diptera: Drosophilidae). Journal of Entomological Science, 55(4). https://doi.org/https://doi.org/10.18474/0749-8004-55.4.560
Guo, X., Yu, Z., & Yin, D. (2023). Sex-dependent obesogenic effect of tetracycline on Drosophila melanogaster deteriorated by dysrhythmia. J Environ Sci (China), 124, 472-480. https://doi.org/10.1016/j.jes.2021.11.029
Hye-Yeon Lee, S.-H. L., Ji-Hyeon Lee, Won-Jae Lee, Kyung-Jin Min. (2019). The role of commensal microbes in the lifespan of Drosophila melanogaster. Aging, 11(13). https://doi.org/10.18632/aging.102073
J. Boulétreau-Merle, R. A., Y. Cohet & J. R. David. (1982). Reproductive strategy in Drosophila melanogaster: Significance of a genetic divergence between temperate and tropical populations. Oecologia 53, 323–329. https://doi.org/https://doi.org/10.1007/BF00389008
James M Kinross , A. W. D. a. J. K. N. (2011). Gut microbiome host interactions in health and disease. Genome Medicine. https://doi.org/https://doi.org/10.1186/gm228
Jaya, A., Wahyudin, E., Djabir, Y. Y., Roska, T. P., Arfiansyah, R., Dirpan, A., & Nainu, F. (2021). Phenotypical Effect of Phosphodiesterase 5 (PDE5) Inhibitor on Behavioral Activities of Fruit Fly Drosophila melanogaster. Biointerface Research in Applied Chemistry, 12(1), 222-229. https://doi.org/10.33263/briac121.222229
Jia, Y., Jin, S., Hu, K., Geng, L., Han, C., Kang, R., Pang, Y., Ling, E., Tan, E. K., Pan, Y., & Liu, W. (2021). Gut microbiome modulates Drosophila aggression through octopamine signaling. Nat Commun, 12(1), 2698. https://doi.org/10.1038/s41467-021-23041-y
Keerthisinghe, T. P., Wang, M., Zhang, Y., Dong, W., & Fang, M. (2019). Low-dose tetracycline exposure alters gut bacterial metabolism and host-immune response: "Personalized" effect? Environ Int, 131, 104989. https://doi.org/10.1016/j.envint.2019.104989
Klein, E. Y., Van Boeckel, T. P., Martinez, E. M., Pant, S., Gandra, S., Levin, S. A., Goossens, H., & Laxminarayan, R. (2018). Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A, 115(15), E3463-E3470. https://doi.org/10.1073/pnas.1717295115
Kummerer, K. (2009). Antibiotics in the aquatic environment a review part I. Chemosphere, 75(4), 417-434. https://doi.org/10.1016/j.chemosphere.2008.11.086
Landis, G. N., Doherty, D., Tower, J. (2020). Analysis of Drosophila melanogaster Lifespan. In: Curran, S. (eds) Aging. Methods in Molecular Biology, 2144. https://doi.org/https://doi.org/10.1007/978-1-0716-0592-9_4
Leftwich, P. T., Clarke, N. V. E., Hutchings, M. I., & Chapman, T. (2017). Gut microbiomes and reproductive isolation in Drosophila. Proc Natl Acad Sci U S A, 114(48), 12767-12772. https://doi.org/10.1073/pnas.1708345114
Leulier, R. C. M. F. (2014). Lactobacilli Host mutualism: learning on the fly. Microb Cell Fact. https://doi.org/https://doi.org/10.1186/1475-2859-13-S1-S6
Liling, S., Puspita Roska, T., Arfiansyah, R., Maryam, F., & Nainu, F. (2021). Pharmacological Effect of Muntingia calabura Leaves on the Expression of sod1 and sod2 in Drosophila. Biointerface Research in Applied Chemistry, 11(5), 12985-12992. https://doi.org/10.33263/briac115.1298512992
Liu, J., Li, X., & Wang, X. (2019). Toxicological effects of ciprofloxacin exposure to Drosophila melanogaster. Chemosphere, 237, 124542. https://doi.org/10.1016/j.chemosphere.2019.124542
Lu, X. M., & Lu, P. Z. (2019). Synergistic effects of key parameters on the fate of antibiotic resistance genes during swine manure composting. Environ Pollut, 252(Pt B), 1277-1287. https://doi.org/10.1016/j.envpol.2019.06.073
Markow, T. A. (2015). Drosophila reproduction: Molecules meet morphology. Proc Natl Acad Sci U S A, 112(27), 8168-8169. https://doi.org/10.1073/pnas.1510121112
Mills, S., Stanton, C., Lane, J. A., Smith, G. J., & Ross, R. P. (2019). Precision Nutrition and the Microbiome, Part I: Current State of the Science. Nutrients, 11(4). https://doi.org/10.3390/nu11040923
Nainu, F., Nakanishi, Y., & Shiratsuchi, A. (2019). Fruit fly as a model organism in the study of human diseases and
drug discovery. J. Cent. Med. Educ. Sapporo Med. Univ, 10, 21-32. https://doi.org/10.15114/jcme.10.21
Nero, L. A., Beloti, V., DE Aguiar Ferreira Barros, M., Ortolani, M. B. T., Tamanini, R., & DE Melo Franco, B. D. G. (2006). Comparison of petrifilm aerobic count plates and de man rogosa sharpe agar for enumeration of lactic acid bacteria. Journal of Rapid Methods & Automation in Microbiology. https://doi.org/https://doi.org/10.1111/j.1745-4581.2006.00050.x
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012). Host-gut microbiota metabolic interactions. Science, 336(6086), 1262-1267. https://doi.org/10.1126/science.1223813
Nikolopoulos, N., Matos, R. C., Ravaud, S., Courtin, P., Akherraz, H., Palussiere, S., Gueguen-Chaignon, V., Salomon-Mallet, M., Guillot, A., Guerardel, Y., Chapot-Chartier, M. P., Grangeasse, C., & Leulier, F. (2023). Structure-function analysis of Lactiplantibacillus plantarum DltE reveals D-alanylated lipoteichoic acids as direct cues supporting Drosophila juvenile growth. Elife, 12. https://doi.org/10.7554/eLife.84669
Osthoff, M., Siegemund, M., Balestra, G., Abdul-Aziz, M. H., & Roberts, J. A. (2016). Prolonged administration of beta lactam antibiotics a comprehensive review and critical appraisal. Swiss Med Wkly, 146, w14368. https://doi.org/10.4414/smw.2016.14368
Pais, I. S., Valente, R. S., Sporniak, M., & Teixeira, L. (2018). Drosophila melanogaster establishes a species specific mutualistic interaction with stable gut colonizing bacteria. PLoS Biol, 16(7), e2005710. https://doi.org/10.1371/journal.pbio.2005710
Panchal, K., & Tiwari, A. K. (2017). Drosophila melanogaster "a potential model organism" for identification of pharmacological properties of plants/plant-derived components. Biomed Pharmacother, 89, 1331-1345. https://doi.org/10.1016/j.biopha.2017.03.001
Quigley, E. M. (2013). Gut Bacteria in Health and Disease. Gastroenterology and Hepatology.
Ramirez, J., Guarner, F., Bustos Fernandez, L., Maruy, A., Sdepanian, V. L., & Cohen, H. (2020). Antibiotics as Major Disruptors of Gut Microbiota. Front Cell Infect Microbiol, 10, 572912. https://doi.org/10.3389/fcimb.2020.572912
Rothschild, D. W., O. Barkan, E. Kurilshikov, A. Korem, T. Zeevi, D. Costea, P. I. Godneva, A. Kalka, I. N. Bar, N. Shilo, S. Lador, D. Vila, A. V. Zmora, N. Pevsner-Fischer, M. Israeli, D. Kosower, N. Malka, G. Wolf, B. C. Avnit-Sagi, T. Lotan-Pompan, M. Weinberger, A. Halpern, Z. Carmi, S. Fu, J. Wijmenga, C. Zhernakova, A. Elinav, E. Segal, E. (2018). Environment dominates over host genetics in shaping human gut microbiota. Nature, 555(7695), 210-215. https://doi.org/10.1038/nature25973
Rumata, N. R., Purwaningsih, D., Asbah, A., As’ad, M. F., Chadran, D., Emran, T. B., & Nainu, F. (2023). Phenotypical and molecular assessments on the pharmacological effects of curcumin in Drosophila melanogaster. Narra J, 3(2). https://doi.org/10.52225/narra.v3i2.117
Sapkota, A., Sapkota, A. R., Kucharski, M., Burke, J., McKenzie, S., Walker, P., & Lawrence, R. (2008). Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int, 34(8), 1215-1226. https://doi.org/10.1016/j.envint.2008.04.009
Schretter, C. E., Vielmetter, J., Bartos, I., Marka, Z., Marka, S., Argade, S., & Mazmanian, S. K. (2018). A gut microbial factor modulates locomotor behaviour in Drosophila. Nature, 563(7731), 402-406. https://doi.org/10.1038/s41586-018-0634-9
Selkrig, J., Mohammad, F., Ng, S. H., Chua, J. Y., Tumkaya, T., Ho, J., Chiang, Y. N., Rieger, D., Pettersson, S., Helfrich-Forster, C., Yew, J. Y., & Claridge-Chang, A. (2018). The Drosophila microbiome has a limited influence on sleep, activity, and courtship behaviors. Sci Rep, 8(1), 10646. https://doi.org/10.1038/s41598-018-28764-5
Siva-Jothy, J. A., Prakash, A., Vasanthakrishnan, R. B., Monteith, K. M., & Vale, P. F. (2018). Oral Bacterial Infection and Shedding in Drosophila melanogaster. J Vis Exp(135). https://doi.org/10.3791/57676
Sommer, F., & Backhed, F. (2013). The gut microbiota masters of host development and physiology. Nat Rev Microbiol, 11(4), 227-238. https://doi.org/10.1038/nrmicro2974
Storelli, G., Defaye, A., Erkosar, B., Hols, P., Royet, J., & Leulier, F. (2011). Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab, 14(3), 403-414. https://doi.org/10.1016/j.cmet.2011.07.012
Sun, M., Ye, M., Jiao, W., Feng, Y., Yu, P., Liu, M., Jiao, J., He, X., Liu, K., Zhao, Y., Wu, J., Jiang, X., & Hu, F. (2018). Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid. J Hazard Mater, 345, 131-139. https://doi.org/10.1016/j.jhazmat.2017.11.036
Syamsidi, A., Rosa, R. A., Sulastri, E., Rahmah, N., Kamri, R. A., Rahma, N., Bin Emran T., Sharma R., Rabaan A. A., Nainu F., Zubair M.S. (2023). Immunomodulatory Effect of Begonia Medicinalis Ethanolic Extract in Drosophila. Biointerface Research in Aplied Chemistry, 13(6). https://doi.org/10.33263/BRIAC136.558
Tafesh-Edwards, G., & Eleftherianos, I. (2023). The role of Drosophila microbiota in gut homeostasis and immunity. Gut Microbes, 15(1), 2208503. https://doi.org/10.1080/19490976.2023.2208503
Vajro, P., Paolella, G., & Fasano, A. (2013). Microbiota and gut-liver axis: their influences on obesity and obesity related liver disease. J Pediatr Gastroenterol Nutr, 56(5), 461-468. https://doi.org/10.1097/MPG.0b013e318284abb5
Vaz, L. E., Kleinman, K. P., Raebel, M. A., Nordin, J. D., Lakoma, M. D., Dutta-Linn, M. M., & Finkelstein, J. A. (2014). Recent trends in outpatient antibiotic use in children. Pediatrics, 133(3), 375-385. https://doi.org/10.1542/peds.2013-2903
Vuong, H. E., Yano, J. M., Fung, T. C., & Hsiao, E. Y. (2017). The microbiome and host behavior. Annu Rev Neurosci, 40, 21-49. https://doi.org/10.1146/annurev-neuro-072116-031347
Wang, Y., Wu, J., Lv, M., Shao, Z., Hungwe, M., Wang, J., Bai, X., Xie, J., Wang, Y., & Geng, W. (2021). Metabolism Characteristics of Lactic Acid Bacteria and the Expanding Applications in Food Industry. Front Bioeng Biotechnol, 9, 612285. https://doi.org/10.3389/fbioe.2021.612285
Weiland, S. O. D., M. Schlick-Steiner, B. C. Steiner, F. M. (2022). Analyses of locomotion, wing morphology, and microbiome in Drosophila nigrosparsa after recovery from antibiotics. Microbiology open, 11(3), e1291. https://doi.org/10.1002/mbo3.1291
World, O. H. (2018). WHO report on surveillance of antibiotic consumption: 2016-2018 early implementation. https://www.who.int/publications/i/item/9789241514880
Yu, Z., Shen, J., Li, Z., Yao, J., Li, W., Xue, L., Vandenberg, L. N., & Yin, D. (2020). Obesogenic effect of Sulfamethoxazole on Drosophila melanogaster with simultaneous disturbances on eclosion rhythm, glucolipid metabolism, and microbiota. Environ Sci Technol, 54(9), 5667-5675. https://doi.org/10.1021/acs.est.9b07889
Zhang, K., Hornef, M. W., & Dupont, A. (2015). The intestinal epithelium as guardian of gut barrier integrity. Cell Microbiol, 17(11), 1561-1569. https://doi.org/10.1111/cmi.12501
Zhang, X. P. a. B. (2021). Environmental Toxicology and Toxicogenomics. Springer Science, 2326. https://doi.org/https://doi.org/10.1007/978-1-0716-1514-0.
Ali, Y. O., Escala, W., Ruan, K., & Zhai, R. G. (2011). Assaying locomotor, learning, and memory deficits in Drosophila models of neurodegeneration. J Vis Exp(49). https://doi.org/10.3791/2504
Ashburner, M., & Roote, J. (2007). Maintenance of a Drosophila Laboratory: General Procedures. Cold Spring Harbor Protocols, 2007(3), pdb.ip35. https://doi.org/10.1101/pdb.ip35
Broderick, N. A., Buchon, N., & Lemaitre, B. (2014). Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. mBio, 5(3), e01117-01114. https://doi.org/10.1128/mBio.01117-14
Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S., & Lemaitre, B. (2009). Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe, 5(2), 200-211. https://doi.org/10.1016/j.chom.2009.01.003
Chao, H., Sun, M., Ye, M., Zheng, X., & Hu, F. (2020). World within world: Intestinal bacteria combining physiological parameters to investigate the response of Metaphire guillelmi to tetracycline stress. Environ Pollut, 261, 114174. https://doi.org/10.1016/j.envpol.2020.114174
Charroux, B., & Royet, J. (2012). Gut-microbiota interactions in non-mammals: what can we learn from Drosophila? Semin Immunol, 24(1), 17-24. https://doi.org/10.1016/j.smim.2011.11.003
Cheng, L., Baonza, A., & Grifoni, D. (2018). Drosophila Models of Human Disease. Biomed Res Int, 2018, 7214974. https://doi.org/10.1155/2018/7214974
Chopra, I., & Roberts, M. (2001). Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev, 65(2), 232-260 ; second page, table of contents. https://doi.org/10.1128/MMBR.65.2.232-260.2001
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O'Connor, E. M., Cusack, S., Harris, H. M., Coakley, M., Lakshminarayanan, B., O'Sullivan, O., Fitzgerald, G. F., Deane, J., O'Connor, M., Harnedy, N., O'Connor, K., O'Mahony, D., van Sinderen, D., Wallace, M., Brennan, L., . . . O'Toole, P. W. (2012). Gut microbiota composition correlates with diet and health in the elderly. Nature, 488(7410), 178-184. https://doi.org/10.1038/nature11319
Clark, R. I., Salazar, A., Yamada, R., Fitz-Gibbon, S., Morselli, M., Alcaraz, J., Rana, A., Rera, M., Pellegrini, M., Ja, W. W., & Walker, D. W. (2015). Distinct Shifts in Microbiota Composition during Drosophila Aging Impair Intestinal Function and Drive Mortality. Cell Rep, 12(10), 1656-1667. https://doi.org/10.1016/j.celrep.2015.08.004
Clark, R. I., & Walker, D. W. (2018). Role of gut microbiota in aging-related health decline: insights from invertebrate models. Cell Mol Life Sci, 75(1), 93-101. https://doi.org/10.1007/s00018-017-2671-1
de Man, J. C., Rogosa, M. and Sharpe, M.E. (1960). A Medium for the Cultivation of Lactobacilli. Journal of Applied Bacteriology, 23, 130-135. https://doi.org/https://doi.org/10.1111/j.1365-2672.1960.tb00188.x
de Vries, L. E., Valles, Y., Agerso, Y., Vaishampayan, P. A., Garcia-Montaner, A., Kuehl, J. V., Christensen, H., Barlow, M., & Francino, M. P. (2011). The gut as reservoir of antibiotic resistance: microbial diversity of tetracycline resistance in mother and infant. PLoS One, 6(6), e21644. https://doi.org/10.1371/journal.pone.0021644
di Cerbo, A., Pezzuto, F., Guidetti, G., Canello, S., & Corsi, L. (2019). Tetracyclines: Insights and Updates of their Use in Human and Animal Pathology and their Potential Toxicity. The Open Biochemistry Journal, 13(1), 1-12. https://doi.org/10.2174/1874091x01913010001
Enabulele, J. E., Chukwumah, N. M., & Enabulele, O. (2020). Tetracycline use in children and knowledge of its oral implications among nursing mothers. Pediatric Dental Journal, 30(3), 224-230. https://doi.org/10.1016/j.pdj.2020.08.003
Fan, Y., & Pedersen, O. (2021). Gut microbiota in human metabolic health and disease. Nat Rev Microbiol, 19(1), 55-71. https://doi.org/10.1038/s41579-020-0433-9
Gebrayel, P. N., C. Al Khodor, S. Bilinski, J. Caselli, E. Comelli, E. M. Egert, M. Giaroni, C. Karpinski, T. M. Loniewski, I. Mulak, A. Reygner, J. Samczuk, P. Serino, M. Sikora, M. Terranegra, A. Ufnal, M. Villeger, R. Pichon, C. Konturek, P. Edeas, M. (2022). Microbiota medicine: towards clinical revolution. J Transl Med, 20(1), 111. https://doi.org/10.1186/s12967-022-03296-9
Gilbert, J. A., Blaser, M. J., Caporaso, J. G., Jansson, J. K., Lynch, S. V., & Knight, R. (2018). Current understanding of the human microbiome. Nat Med, 24(4), 392-400. https://doi.org/10.1038/nm.4517
Gökçe Üstündağ, K. B., Ender Büyükgüzel. (2020). Penicillin Impact on Survivorship, Development, and Adult Longevity of Drosophila melanogaster (Diptera: Drosophilidae). Journal of Entomological Science, 55(4). https://doi.org/https://doi.org/10.18474/0749-8004-55.4.560
Guo, X., Yu, Z., & Yin, D. (2023). Sex-dependent obesogenic effect of tetracycline on Drosophila melanogaster deteriorated by dysrhythmia. J Environ Sci (China), 124, 472-480. https://doi.org/10.1016/j.jes.2021.11.029
Hye-Yeon Lee, S.-H. L., Ji-Hyeon Lee, Won-Jae Lee, Kyung-Jin Min. (2019). The role of commensal microbes in the lifespan of Drosophila melanogaster. Aging, 11(13). https://doi.org/10.18632/aging.102073
J. Boulétreau-Merle, R. A., Y. Cohet & J. R. David. (1982). Reproductive strategy in Drosophila melanogaster: Significance of a genetic divergence between temperate and tropical populations. Oecologia 53, 323–329. https://doi.org/https://doi.org/10.1007/BF00389008
James M Kinross , A. W. D. a. J. K. N. (2011). Gut microbiome host interactions in health and disease. Genome Medicine. https://doi.org/https://doi.org/10.1186/gm228
Jaya, A., Wahyudin, E., Djabir, Y. Y., Roska, T. P., Arfiansyah, R., Dirpan, A., & Nainu, F. (2021). Phenotypical Effect of Phosphodiesterase 5 (PDE5) Inhibitor on Behavioral Activities of Fruit Fly Drosophila melanogaster. Biointerface Research in Applied Chemistry, 12(1), 222-229. https://doi.org/10.33263/briac121.222229
Jia, Y., Jin, S., Hu, K., Geng, L., Han, C., Kang, R., Pang, Y., Ling, E., Tan, E. K., Pan, Y., & Liu, W. (2021). Gut microbiome modulates Drosophila aggression through octopamine signaling. Nat Commun, 12(1), 2698. https://doi.org/10.1038/s41467-021-23041-y
Keerthisinghe, T. P., Wang, M., Zhang, Y., Dong, W., & Fang, M. (2019). Low-dose tetracycline exposure alters gut bacterial metabolism and host-immune response: "Personalized" effect? Environ Int, 131, 104989. https://doi.org/10.1016/j.envint.2019.104989
Klein, E. Y., Van Boeckel, T. P., Martinez, E. M., Pant, S., Gandra, S., Levin, S. A., Goossens, H., & Laxminarayan, R. (2018). Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A, 115(15), E3463-E3470. https://doi.org/10.1073/pnas.1717295115
Kummerer, K. (2009). Antibiotics in the aquatic environment a review part I. Chemosphere, 75(4), 417-434. https://doi.org/10.1016/j.chemosphere.2008.11.086
Landis, G. N., Doherty, D., Tower, J. (2020). Analysis of Drosophila melanogaster Lifespan. In: Curran, S. (eds) Aging. Methods in Molecular Biology, 2144. https://doi.org/https://doi.org/10.1007/978-1-0716-0592-9_4
Leftwich, P. T., Clarke, N. V. E., Hutchings, M. I., & Chapman, T. (2017). Gut microbiomes and reproductive isolation in Drosophila. Proc Natl Acad Sci U S A, 114(48), 12767-12772. https://doi.org/10.1073/pnas.1708345114
Leulier, R. C. M. F. (2014). Lactobacilli Host mutualism: learning on the fly. Microb Cell Fact. https://doi.org/https://doi.org/10.1186/1475-2859-13-S1-S6
Liling, S., Puspita Roska, T., Arfiansyah, R., Maryam, F., & Nainu, F. (2021). Pharmacological Effect of Muntingia calabura Leaves on the Expression of sod1 and sod2 in Drosophila. Biointerface Research in Applied Chemistry, 11(5), 12985-12992. https://doi.org/10.33263/briac115.1298512992
Liu, J., Li, X., & Wang, X. (2019). Toxicological effects of ciprofloxacin exposure to Drosophila melanogaster. Chemosphere, 237, 124542. https://doi.org/10.1016/j.chemosphere.2019.124542
Lu, X. M., & Lu, P. Z. (2019). Synergistic effects of key parameters on the fate of antibiotic resistance genes during swine manure composting. Environ Pollut, 252(Pt B), 1277-1287. https://doi.org/10.1016/j.envpol.2019.06.073
Markow, T. A. (2015). Drosophila reproduction: Molecules meet morphology. Proc Natl Acad Sci U S A, 112(27), 8168-8169. https://doi.org/10.1073/pnas.1510121112
Mills, S., Stanton, C., Lane, J. A., Smith, G. J., & Ross, R. P. (2019). Precision Nutrition and the Microbiome, Part I: Current State of the Science. Nutrients, 11(4). https://doi.org/10.3390/nu11040923
Nainu, F., Nakanishi, Y., & Shiratsuchi, A. (2019). Fruit fly as a model organism in the study of human diseases and
drug discovery. J. Cent. Med. Educ. Sapporo Med. Univ, 10, 21-32. https://doi.org/10.15114/jcme.10.21
Nero, L. A., Beloti, V., DE Aguiar Ferreira Barros, M., Ortolani, M. B. T., Tamanini, R., & DE Melo Franco, B. D. G. (2006). Comparison of petrifilm aerobic count plates and de man rogosa sharpe agar for enumeration of lactic acid bacteria. Journal of Rapid Methods & Automation in Microbiology. https://doi.org/https://doi.org/10.1111/j.1745-4581.2006.00050.x
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012). Host-gut microbiota metabolic interactions. Science, 336(6086), 1262-1267. https://doi.org/10.1126/science.1223813
Nikolopoulos, N., Matos, R. C., Ravaud, S., Courtin, P., Akherraz, H., Palussiere, S., Gueguen-Chaignon, V., Salomon-Mallet, M., Guillot, A., Guerardel, Y., Chapot-Chartier, M. P., Grangeasse, C., & Leulier, F. (2023). Structure-function analysis of Lactiplantibacillus plantarum DltE reveals D-alanylated lipoteichoic acids as direct cues supporting Drosophila juvenile growth. Elife, 12. https://doi.org/10.7554/eLife.84669
Osthoff, M., Siegemund, M., Balestra, G., Abdul-Aziz, M. H., & Roberts, J. A. (2016). Prolonged administration of beta lactam antibiotics a comprehensive review and critical appraisal. Swiss Med Wkly, 146, w14368. https://doi.org/10.4414/smw.2016.14368
Pais, I. S., Valente, R. S., Sporniak, M., & Teixeira, L. (2018). Drosophila melanogaster establishes a species specific mutualistic interaction with stable gut colonizing bacteria. PLoS Biol, 16(7), e2005710. https://doi.org/10.1371/journal.pbio.2005710
Panchal, K., & Tiwari, A. K. (2017). Drosophila melanogaster "a potential model organism" for identification of pharmacological properties of plants/plant-derived components. Biomed Pharmacother, 89, 1331-1345. https://doi.org/10.1016/j.biopha.2017.03.001
Quigley, E. M. (2013). Gut Bacteria in Health and Disease. Gastroenterology and Hepatology.
Ramirez, J., Guarner, F., Bustos Fernandez, L., Maruy, A., Sdepanian, V. L., & Cohen, H. (2020). Antibiotics as Major Disruptors of Gut Microbiota. Front Cell Infect Microbiol, 10, 572912. https://doi.org/10.3389/fcimb.2020.572912
Rothschild, D. W., O. Barkan, E. Kurilshikov, A. Korem, T. Zeevi, D. Costea, P. I. Godneva, A. Kalka, I. N. Bar, N. Shilo, S. Lador, D. Vila, A. V. Zmora, N. Pevsner-Fischer, M. Israeli, D. Kosower, N. Malka, G. Wolf, B. C. Avnit-Sagi, T. Lotan-Pompan, M. Weinberger, A. Halpern, Z. Carmi, S. Fu, J. Wijmenga, C. Zhernakova, A. Elinav, E. Segal, E. (2018). Environment dominates over host genetics in shaping human gut microbiota. Nature, 555(7695), 210-215. https://doi.org/10.1038/nature25973
Rumata, N. R., Purwaningsih, D., Asbah, A., As’ad, M. F., Chadran, D., Emran, T. B., & Nainu, F. (2023). Phenotypical and molecular assessments on the pharmacological effects of curcumin in Drosophila melanogaster. Narra J, 3(2). https://doi.org/10.52225/narra.v3i2.117
Sapkota, A., Sapkota, A. R., Kucharski, M., Burke, J., McKenzie, S., Walker, P., & Lawrence, R. (2008). Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int, 34(8), 1215-1226. https://doi.org/10.1016/j.envint.2008.04.009
Schretter, C. E., Vielmetter, J., Bartos, I., Marka, Z., Marka, S., Argade, S., & Mazmanian, S. K. (2018). A gut microbial factor modulates locomotor behaviour in Drosophila. Nature, 563(7731), 402-406. https://doi.org/10.1038/s41586-018-0634-9
Selkrig, J., Mohammad, F., Ng, S. H., Chua, J. Y., Tumkaya, T., Ho, J., Chiang, Y. N., Rieger, D., Pettersson, S., Helfrich-Forster, C., Yew, J. Y., & Claridge-Chang, A. (2018). The Drosophila microbiome has a limited influence on sleep, activity, and courtship behaviors. Sci Rep, 8(1), 10646. https://doi.org/10.1038/s41598-018-28764-5
Siva-Jothy, J. A., Prakash, A., Vasanthakrishnan, R. B., Monteith, K. M., & Vale, P. F. (2018). Oral Bacterial Infection and Shedding in Drosophila melanogaster. J Vis Exp(135). https://doi.org/10.3791/57676
Sommer, F., & Backhed, F. (2013). The gut microbiota masters of host development and physiology. Nat Rev Microbiol, 11(4), 227-238. https://doi.org/10.1038/nrmicro2974
Storelli, G., Defaye, A., Erkosar, B., Hols, P., Royet, J., & Leulier, F. (2011). Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab, 14(3), 403-414. https://doi.org/10.1016/j.cmet.2011.07.012
Sun, M., Ye, M., Jiao, W., Feng, Y., Yu, P., Liu, M., Jiao, J., He, X., Liu, K., Zhao, Y., Wu, J., Jiang, X., & Hu, F. (2018). Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid. J Hazard Mater, 345, 131-139. https://doi.org/10.1016/j.jhazmat.2017.11.036
Syamsidi, A., Rosa, R. A., Sulastri, E., Rahmah, N., Kamri, R. A., Rahma, N., Bin Emran T., Sharma R., Rabaan A. A., Nainu F., Zubair M.S. (2023). Immunomodulatory Effect of Begonia Medicinalis Ethanolic Extract in Drosophila. Biointerface Research in Aplied Chemistry, 13(6). https://doi.org/10.33263/BRIAC136.558
Tafesh-Edwards, G., & Eleftherianos, I. (2023). The role of Drosophila microbiota in gut homeostasis and immunity. Gut Microbes, 15(1), 2208503. https://doi.org/10.1080/19490976.2023.2208503
Vajro, P., Paolella, G., & Fasano, A. (2013). Microbiota and gut-liver axis: their influences on obesity and obesity related liver disease. J Pediatr Gastroenterol Nutr, 56(5), 461-468. https://doi.org/10.1097/MPG.0b013e318284abb5
Vaz, L. E., Kleinman, K. P., Raebel, M. A., Nordin, J. D., Lakoma, M. D., Dutta-Linn, M. M., & Finkelstein, J. A. (2014). Recent trends in outpatient antibiotic use in children. Pediatrics, 133(3), 375-385. https://doi.org/10.1542/peds.2013-2903
Vuong, H. E., Yano, J. M., Fung, T. C., & Hsiao, E. Y. (2017). The microbiome and host behavior. Annu Rev Neurosci, 40, 21-49. https://doi.org/10.1146/annurev-neuro-072116-031347
Wang, Y., Wu, J., Lv, M., Shao, Z., Hungwe, M., Wang, J., Bai, X., Xie, J., Wang, Y., & Geng, W. (2021). Metabolism Characteristics of Lactic Acid Bacteria and the Expanding Applications in Food Industry. Front Bioeng Biotechnol, 9, 612285. https://doi.org/10.3389/fbioe.2021.612285
Weiland, S. O. D., M. Schlick-Steiner, B. C. Steiner, F. M. (2022). Analyses of locomotion, wing morphology, and microbiome in Drosophila nigrosparsa after recovery from antibiotics. Microbiology open, 11(3), e1291. https://doi.org/10.1002/mbo3.1291
World, O. H. (2018). WHO report on surveillance of antibiotic consumption: 2016-2018 early implementation. https://www.who.int/publications/i/item/9789241514880
Yu, Z., Shen, J., Li, Z., Yao, J., Li, W., Xue, L., Vandenberg, L. N., & Yin, D. (2020). Obesogenic effect of Sulfamethoxazole on Drosophila melanogaster with simultaneous disturbances on eclosion rhythm, glucolipid metabolism, and microbiota. Environ Sci Technol, 54(9), 5667-5675. https://doi.org/10.1021/acs.est.9b07889
Zhang, K., Hornef, M. W., & Dupont, A. (2015). The intestinal epithelium as guardian of gut barrier integrity. Cell Microbiol, 17(11), 1561-1569. https://doi.org/10.1111/cmi.12501
Zhang, X. P. a. B. (2021). Environmental Toxicology and Toxicogenomics. Springer Science, 2326. https://doi.org/https://doi.org/10.1007/978-1-0716-1514-0.
Published
2024-09-25
How to Cite
Saadjad, Z. P., Sartini, S., Chairatunnisa, R., Latada, N. P., Mudjahid, M., & Nainu, F. (2024). Gut Microbiota Dynamics and Phenotypic Changes Induced by Tetracycline in Drosophila melanogaster. Indonesian Journal of Pharmacy, 35(3), 437–450. https://doi.org/10.22146/ijp.11076
Issue
Section
Research Article
