Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons

ABSTRACTProbiotics are live microorganisms that offer potential benefits to their hosts and can occasionally influence behavioral responses. However, the detailed mechanisms by which probiotics affect the behavior of their hosts and the underlying biogenic effects remain unclear. Lactic acid bacteri...

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Main Authors: Shuk-Man Ho, Wan-Hua Tsai, Chih-Ho Lai, Meng-Hsuan Chiang, Wang-Po Lee, Hui-Yu Wu, Pei-Yi Bai, Tony Wu, Chia-Lin Wu
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2024.2316533
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author Shuk-Man Ho
Wan-Hua Tsai
Chih-Ho Lai
Meng-Hsuan Chiang
Wang-Po Lee
Hui-Yu Wu
Pei-Yi Bai
Tony Wu
Chia-Lin Wu
author_facet Shuk-Man Ho
Wan-Hua Tsai
Chih-Ho Lai
Meng-Hsuan Chiang
Wang-Po Lee
Hui-Yu Wu
Pei-Yi Bai
Tony Wu
Chia-Lin Wu
author_sort Shuk-Man Ho
collection DOAJ
description ABSTRACTProbiotics are live microorganisms that offer potential benefits to their hosts and can occasionally influence behavioral responses. However, the detailed mechanisms by which probiotics affect the behavior of their hosts and the underlying biogenic effects remain unclear. Lactic acid bacteria, specifically Lactobacillus spp. are known probiotics. Drosophila melanogaster, commonly known as the fruit fly, is a well-established model organism for investigating the interaction between the host and gut microbiota in translational research. Herein, we showed that 5-day administration of Lactobacillus acidophilus (termed GMNL-185) or Lacticaseibacillus rhamnosus (termed GMNL-680) enhances olfactory-associative memory in Drosophila. Moreover, a combined diet of GMNL-185 and GMNL-680 demonstrated synergistic effects on memory functions. Live brain imaging revealed a significant increase in calcium responses to the training odor in the mushroom body β and γ lobes of flies that underwent mixed feeding with GMNL-185 and GMNL-680. Quantitative reverse transcription polymerase chain reaction (qRT-PCR) and whole-mount brain immunohistochemistry revealed significant upregulation of lactate dehydrogenase (LDH) expression in the fly brain following the mixed feeding. Notably, the genetic knockdown of Ldh in neurons, specifically in mushroom body, ameliorated the beneficial effects of mixed feeding with GMNL-185 and GMNL-680 on memory improvement. Altogether, our results demonstrate that supplementation with L. acidophilus and L. rhamnosus enhances memory functions in flies by increasing brain LDH levels.
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spelling doaj.art-a5f7d8e4921c456dabd74d14afb6b57a2024-02-19T15:56:24ZengTaylor & Francis GroupGut Microbes1949-09761949-09842024-12-0116110.1080/19490976.2024.2316533Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neuronsShuk-Man Ho0Wan-Hua Tsai1Chih-Ho Lai2Meng-Hsuan Chiang3Wang-Po Lee4Hui-Yu Wu5Pei-Yi Bai6Tony Wu7Chia-Lin Wu8Department of Biochemistry, Department of Microbiology and Immunology, Graduate Institute of Biomedical Sciences, Department of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanResearch and Development Department, GenMont Biotech Incorporation, Tainan, TaiwanDepartment of Biochemistry, Department of Microbiology and Immunology, Graduate Institute of Biomedical Sciences, Department of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Biochemistry, Department of Microbiology and Immunology, Graduate Institute of Biomedical Sciences, Department of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Biochemistry, Department of Microbiology and Immunology, Graduate Institute of Biomedical Sciences, Department of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Biochemistry, Department of Microbiology and Immunology, Graduate Institute of Biomedical Sciences, Department of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Biochemistry, Department of Microbiology and Immunology, Graduate Institute of Biomedical Sciences, Department of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Neurology, New Taipei Municipal TuCheng Hospital, Chang Gung Memorial Hospital, New Taipei City, TaiwanDepartment of Biochemistry, Department of Microbiology and Immunology, Graduate Institute of Biomedical Sciences, Department of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanABSTRACTProbiotics are live microorganisms that offer potential benefits to their hosts and can occasionally influence behavioral responses. However, the detailed mechanisms by which probiotics affect the behavior of their hosts and the underlying biogenic effects remain unclear. Lactic acid bacteria, specifically Lactobacillus spp. are known probiotics. Drosophila melanogaster, commonly known as the fruit fly, is a well-established model organism for investigating the interaction between the host and gut microbiota in translational research. Herein, we showed that 5-day administration of Lactobacillus acidophilus (termed GMNL-185) or Lacticaseibacillus rhamnosus (termed GMNL-680) enhances olfactory-associative memory in Drosophila. Moreover, a combined diet of GMNL-185 and GMNL-680 demonstrated synergistic effects on memory functions. Live brain imaging revealed a significant increase in calcium responses to the training odor in the mushroom body β and γ lobes of flies that underwent mixed feeding with GMNL-185 and GMNL-680. Quantitative reverse transcription polymerase chain reaction (qRT-PCR) and whole-mount brain immunohistochemistry revealed significant upregulation of lactate dehydrogenase (LDH) expression in the fly brain following the mixed feeding. Notably, the genetic knockdown of Ldh in neurons, specifically in mushroom body, ameliorated the beneficial effects of mixed feeding with GMNL-185 and GMNL-680 on memory improvement. Altogether, our results demonstrate that supplementation with L. acidophilus and L. rhamnosus enhances memory functions in flies by increasing brain LDH levels.https://www.tandfonline.com/doi/10.1080/19490976.2024.2316533ProbioticsLactobacillusBrainOlfactory memoryLactate dehydrogenaseDrosophila melanogaster
spellingShingle Shuk-Man Ho
Wan-Hua Tsai
Chih-Ho Lai
Meng-Hsuan Chiang
Wang-Po Lee
Hui-Yu Wu
Pei-Yi Bai
Tony Wu
Chia-Lin Wu
Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons
Gut Microbes
Probiotics
Lactobacillus
Brain
Olfactory memory
Lactate dehydrogenase
Drosophila melanogaster
title Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons
title_full Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons
title_fullStr Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons
title_full_unstemmed Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons
title_short Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons
title_sort probiotic lactobacillus spp improves drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons
topic Probiotics
Lactobacillus
Brain
Olfactory memory
Lactate dehydrogenase
Drosophila melanogaster
url https://www.tandfonline.com/doi/10.1080/19490976.2024.2316533
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