Potential effect of Escherichia coli Shiga toxin metabolites in the induction of cognitive dysfunction and stress memory formation in naïve goldfish Carassius auratus
Article Main
Abstract
The oral-gut-brain (OGB) axis is a three-way communication process that forms cognitive functions, especially learning and memory (LM) formation. Recent studies showed that the OGB axis is pivotal in efficiently forming and regulating the brain homeostasis mechanism. In this OGB axis, oral and gut commensals play a major role in the bidirectional communication with the brain through the blood-brain barrier (BBB). The dysbiosis of oral and gut commensals results in cognitive dysfunctions like cognitive decline. The present study aimed to study the effect of Escherichia coli induced oral-gut dysbiosis on cognitive memory (CM) formation with the help of a cue-based learning paradigm (CBLP). Other than CM formation, stress memory (SM) formation was also studied with the help of behavioural paradigms like predator exposure test (PET), light and dark box test (LDBT), and open field test (OFT) in naïve goldfish Carassius auratus. The results of the study proved that the OGB axis is possibly involved in the formation of CM by inhibiting stress formation in a habituated, serene environment. Behavioural responses of E. coli-infused groups showed that higher colonization/accumulation of E. coli results in the formation of cognitive decline through the release of shiga toxin (ST) metabolites. It also showed that the release of ST metabolites may disrupt gut dysbiosis through the development of gastroenteritis. Developed gastroenteritis further results in cognitive memory - decline (70-75 %) due to the long-term existence of E. coli-induced oral/gut dysbiosis. Thus, the present study stated the possible effect of E. coli shiga toxin metabolites on the development of cognitive dysfunction in a unique manner.
Article Details
Article Details
Keywords
Cognition, Escherichia coli, Oral-gut-brain axis, Shiga toxin metabolites, Stress memory
References
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Mukilan, M. (2024b). Pyocyanin: A virulence factor of Pseudomonas aeruginosa in the disruption of brain homeostasis regulation in gold fish Carassius auratus. J. Appl. & Nat. Sci., 16(3), 949-963. https://doi.org/10.31018/jans.v16i3.5393.
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Mukilan, M., Elakkiya, V., Darshini, M. & Varshini, M. (2024b). Exploring the Potential Role of Lactobacillus plantarum in the Reversal of Induced Cognitive Long-term Memory Impairment, Journal of Experimental Biology and Agricultural Sciences, 12(2), 175-187. https://doi.org/10.18006/2024.12(2).175.187.
Mukilan, M., Antony Mathew, M.T., Yaswanth, S. & Mallikarjun, V. (2024c). Role of Probiotic Strain Lactobacillus acidophilus in the Reversal of Gut Dysbiosis Induced Brain Cognitive Decline, Journal of Experimental Biology and Agricultural Sciences, 12(1), 36-48. https://doi.org/10.18006/2024.12(1).36.48.
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Noe, C.R., Noe-Letschnig, M., Handschuh, P., Noe, C.A. & Lanzenberger, R. (2020). Dysfunction of the Blood-Brain Barrier – A Key Step in Neurodegeneration and Dementia, Front. Aging Neurosci., 12, 185. https://doi.org/10.3389/fnagi.2020.00185.
Piccioni, A., Covino, M., Candelli, M., Ojetti, V., Capacci, A., Gasbarrini, A., Franceschi, F. & Merra, G. (2023). How Do Diet Patterns, Single Foods, Prebiotics and Probiotics Impact Gut Microbiota? Microbiology Research, 14(1), 390-408. https://doi.org/10.3390/microbiolres14010030.
Pitchaikani, S., Mukilan, M., Govindan, P., Kathiravan, G. & Shakila, H. (2024). Highlighting the Importance of Matrix Metalloproteinase 1, 8, and 9 Expression during the Progression of Mycobacterium tuberculosis Infection, Journal of Experimental Biology and Agricultural Sciences, 12(1), 49-59. https://doi.org/10.18006/2024.12(1).49.59.
Rajan K.E. (2021). Olfactory learning and memory in the greater short-nosed fruit bat Cynopterus sphinx: the influence of conspecifics distress calls, Journal of Comparative physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 207(5), 667-679. https://doi.org/10.1007/s00359-021-01505-2.
Rashidi S.K., Kalirad A., Rafie S., Behzad E. & Dezfouli M.A. (2023). The role of microRNAs in neurobiology and pathophysiology of the hippocampus, Front. Mol. Neurosci., 16, 1226413. https://doi.org/10.3389/fnmol.2023.1226413.
Said-Sadier, N., Sayegh, B., Farah, R., Abbas, L.A., Dweik, R., Tang, N. & Ojcius, D.M. (2023). Association between Periodontal Disease and Cognitive Impairment in Adults, Int. J. Environ. Res. Public Health, 20(6), 4707. https://doi.org/10.3390/ijerph20064707.
Sansores-España, L.D., Melgar-Rodríguez, S., Olivares-Sagredo, K., Cafferata, E.A., Martínez-Aguilar, V.M., Vernal, R., Paula-Lima, A.C. & Díaz-Zúñiga J. (2021). Oral-Gut-Brain Axis in Experimental Models of Periodontitis: Associating Gut Dysbiosis with Neurodegenerative Diseases, Front. Aging, 2, 781582. https://doi.org/10.3389/fragi.2021.781582.
Schütze, S., Döpke, A., Kellert, B., Seele, J., Ballüer, M., Bunkowski, S., Kreutzfeldt, M., Brück, W. & Nau, R. (2022). Intracerebral Infection with E. coli Impairs Spatial Learning and Induces Necrosis of Hippocampal Neurons in the Tg2576 Mouse Model of Alzheimer’s Disease, J. Alzheimer’s Dis. Rep., 6(1), 101-114. https://doi.org/10.3233/ADR-210049.
Shahbazi A., Sepehrinezhad A., Vahdani E., Jamali R., Ghasempour M., Massoudian S., Negah S.S. & Larsen F.S. (2023). Gut Dysbiosis and Blood-Brain Barrier Alteration in Hepatic Encephalopathy: From Gut to Brain, Biomedicines, 11(5), 1272. https://doi.org/10.3390/biomedicines11051272.
Squarzanti D.F., Dell’Atti F., Scalia A.C., Najmi Z., Cochis A. & Malfa P. (2024). Exploring the In Vitro Antibacterial Potential of Specific Probiotic Strains against Oral Pathogens, Microorganisms, 12(3), 441. https://doi.org/10.3390/microorganisms12030441.
Thangaleela S., Shanmugapriya V., Mukilan M., Radhakrishnan K. & Rajan K.E. (2018). Alterations in MicroRNA-132/212 Expression Impairs Fear Memory in Goldfish Carassius auratus, Ann. Neurosci., 25(2), 90-97. https://doi.org/10.1159/000486842.
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Anand, N., Gorantla, V.R. & Chidambaram, S.B. (2023). The Role of Gut Dysbiosis in the Pathophysiology of Neuropsychiatric Disorders, Cells, 12(1), 54. https://doi.org/10.3390/cells12010054.
Anjana, & Tiwari, S.K. (2022). Bacteriocin-Producing Probiotic Lactic Acid Bacteria in Controlling Dysbiosis of the Gut Microbiota, Front. Cell. Infect. Microbiol., 12, 851140. https://doi.org/10.3389/fcimb.2022.851140.
Chen, Y., Xu, J. & Chen, Y. (2021). Regulation of Neurotransmitters by the Gut Microbiota and Effects on Cognition in Neurological Disorders, Nutrients, 13(6), 2099. https://doi.org/10.3390/nu13062099.
Dicks, L.M.T. (2022). Gut Bacteria and Neurotransmitters, Microorganisms, 10(9), 1838. https://doi.org/10.3390/microorganisms10091838.
Elghannam, M.T., Hassanien, M.H., Ameen, Y.A., Turky, E.A., ELattar, G.M., ELRay, A.A. & ELTalkawy, M.D. (2024). Oral microbiome dysbiosis and gastrointestinal diseases: a narrative review, Egyptian Liver Journal, 14, 32. https://doi.org/10.1186/s43066-024-00340-9.
Ganesh, A., Bogdanowicz, W., Balamurugan, K., Varman, D.R. & Rajan, K.E. (2012). Egr -1 antisense oligodeoxynucleotide administration into the greater short-nosed fruit bat Cynopterus sphinx, Brain Res., 14471, 33-45. https://doi.org/10.1016/j.brainres.2012.06.038.
Ganesh, A., Bogdanowicz, W., Haupt, M., Marimuthu, G. & Rajan, K.E. (2010). Role of olfactory bulb serotonin in olfactory learning in the greater short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae), Brain Res., 1352, 108-117. https://doi.org/10.1016/j.brainres.2010.06.058.
Georges, F.M., Do, N.T. & Seleem, D. (2022). Oral dysbiosis and systemic diseases, Front. Dent. Med., 3, 995423. https://doi.org/10.3389/fdmed.2022.9 95423.
Heravi, F.S. & Hu, H. (2023). Bifidobacterium: Host-Microbiome Interaction and Mechanism of Action in Preventing Common Gut-Microbiota-Associated Complications in Preterm Infants: A Narrative Review, Nutrients, 15(3), 709. https://doi.org/10.3390/nu15030709.
Kim, J., Lee, K., Lee, S., Jang, H. & Kim, D. (2020). Interplay Between Human Gut Bacteria Escherichia coli and Lactobacillus mucosae in the Occurrence of Neuropsychiatric Disorders in Mice, Front. Immunol., 11, 273. https://doi.org/10.3389/fimmu.2020.00273.
Kolobaric, A., Andreescu, C., Jašarević, E., Hong, C.H., Roh, H.W., Cheong, J.Y., Kim, Y.K., Shin, T.S., Kang, C.S., Kwon, C.O., Yoon, S.Y., Hong, S.W., Aizenstein, H.J., Karim, H.T. & Son, S.J. (2024). Gut microbiome predicts cognitive function and depressive symptoms in late life, Mol.Psychiatry, https://doi.org/ 10.1038/s41380-024-02551-3.
Lee, K., Jeong, Y. & Lee, M. (2021). Escherichia coli Shiga Toxins and Gut Microbiota Interactions, Toxins, 13(6), 416. https://doi.org/ 10.3390/toxins13060416.
Li, R., Wang, J., Xiong, W., Luo, Y., Feng, H., Zhou, H., Peng, Y., He, Y. & Ye, Q. (2024). The oral-brain axis: can periodontal pathogens trigger the onset and progression of Alzheimer’s disease? Front. Microbiol., 15, 1358179. https://doi.org/10.3389/fmicb.2024.1358179.
Monday, H.R., Kharod, S.C., Yoon, Y.J., Singer, R.H. & Castillo, P.E. (2022). Presynaptic FMRP and local protein synthesis support structural and functional plasticity of glutamatergic axon terminals, Neurons, 110, 2588-2606. https://doi.org/10.1016/j.neuron.2022.05.024.
Morozova, A., Zorkina, Y., Abramova, O., Pavlova, O., Pavlov, K., Soloveva, K., Volkova, M., Alekseeva, P., Andryshchenko, A., Kostyuk, G., Gurina, O. & Chekhonin, V. (2022). Neurobiological Highlights of Cognitive Impairment in Psychiatric Disorders, Int. J. Mol. Sci., 23(3), 1217. https://doi.org/10.3390/ijms23031217.
Mukilan, M. (2025a). Oral-Gut Dysbiosis: Causative for the Initiation of Brain Cognitive Memory Decline. Res. J. Biotech., 20(3), 254-262. https://doi.org/10.25 303/203rjbt2540262.
Mukilan, M. (2025b). Impact of Antibiotic Oral Infusions on the Development of Cognitive Dysfunctions. Res. J. Biotech., 20(2), 183-194. https://doi.org/10.25303/20 2rjbt1830194.
Mukilan, M. (2025c). Probiotic Strain Lactobacillus fermentum as a Potential Agent for the Reversal of Non-Periodontal Microorganisms Induced Cognitive Dysfunctions. Res. J. Biotech., 20(1), 55-68. https://doi.org/10.25303/201rjbt055068.
Mukilan, M. (2024a). Impact of Oral Non-periodontal Pathogens (Klebsiella pneumonia, Streptococcus pneumonia and Staphylococcus aureus) in the induction of Cognitive Memory Impairment. Res. J. Biotech., 19(12), 151-162. https://doi.org/10.25303/1912rjbt1510162.
Mukilan, M. (2024b). Pyocyanin: A virulence factor of Pseudomonas aeruginosa in the disruption of brain homeostasis regulation in gold fish Carassius auratus. J. Appl. & Nat. Sci., 16(3), 949-963. https://doi.org/10.31018/jans.v16i3.5393.
Mukilan, M., Adithya, R. & Pruthivi, S. (2024a). Role of Probiotic Microorganisms in the Brain Plasticity Development. Journal of Experimental Biology and Agricultural Sciences, 12(3), 354-365. https://doi.org/10.18 006/2024.12(3).354.365.
Mukilan, M., Elakkiya, V., Darshini, M. & Varshini, M. (2024b). Exploring the Potential Role of Lactobacillus plantarum in the Reversal of Induced Cognitive Long-term Memory Impairment, Journal of Experimental Biology and Agricultural Sciences, 12(2), 175-187. https://doi.org/10.18006/2024.12(2).175.187.
Mukilan, M., Antony Mathew, M.T., Yaswanth, S. & Mallikarjun, V. (2024c). Role of Probiotic Strain Lactobacillus acidophilus in the Reversal of Gut Dysbiosis Induced Brain Cognitive Decline, Journal of Experimental Biology and Agricultural Sciences, 12(1), 36-48. https://doi.org/10.18006/2024.12(1).36.48.
Mukilan, M. (2023). Impact of Pseudomonas aeruginosa, Bacillus subtilis, Staphylococcus aureus, and Escherichia coli Oral Infusions on Cognitive Memory Decline in Mild Cognitive Impairment, Journal of Experimental Biology and Agricultural Sciences, 11(3), 581-592. https://doi.org/10.18006/2023.11(3).581.592.
Mukilan, M. (2022). Effects of Probiotics, Prebiotics and Synbiotic Supplementation on Cognitive Impairment: A Review, Journal of Experimental Biology and Agricultural Sciences, 10(1), 1-11. https://doi.org/10.18006/2023.10(1).1.11.
Mukilan, M., Bogdanowicz, W., Marimuthu, G. & Rajan, K.E. (2018a). Odour discrimination learning in the Indian greater short-nosed fruit bat (Cynopterus sphinx): differential expression of Egr-1, C-fos and PP-1 in the olfactory bulb, amygdala and hippocampus, J. Exp. Biol., 221(Pt 12), jeb175364. https://doi.org/10.1242/jeb.175364.
Mukilan, M., Rajathei, D.M., Jeyaraj, E., Kayalvizhi, N. & Rajan, K.E. (2018b). MiR-132 regulated olfactory bulb proteins linked to olfactory learning in greater short-nosed fruit bat Cynopterus sphinx, Gene, 671, 10-20. https://doi.org/10.1016/j.gene.2018.05.107.
Mukilan, M., Varman, D.R., Sudhakar, S. & Rajan, K.E. (2015). Activity-dependent expression of miR-132 regulates immediate early gene induction during olfactory learning in the greater short-nosed fruit bat, Cynopterus sphinx, Neurobiol. Learn. Mem., 120, 41-51. https://doi.org/10.1016/j.nlm.2015.02.010.
Noe, C.R., Noe-Letschnig, M., Handschuh, P., Noe, C.A. & Lanzenberger, R. (2020). Dysfunction of the Blood-Brain Barrier – A Key Step in Neurodegeneration and Dementia, Front. Aging Neurosci., 12, 185. https://doi.org/10.3389/fnagi.2020.00185.
Piccioni, A., Covino, M., Candelli, M., Ojetti, V., Capacci, A., Gasbarrini, A., Franceschi, F. & Merra, G. (2023). How Do Diet Patterns, Single Foods, Prebiotics and Probiotics Impact Gut Microbiota? Microbiology Research, 14(1), 390-408. https://doi.org/10.3390/microbiolres14010030.
Pitchaikani, S., Mukilan, M., Govindan, P., Kathiravan, G. & Shakila, H. (2024). Highlighting the Importance of Matrix Metalloproteinase 1, 8, and 9 Expression during the Progression of Mycobacterium tuberculosis Infection, Journal of Experimental Biology and Agricultural Sciences, 12(1), 49-59. https://doi.org/10.18006/2024.12(1).49.59.
Rajan K.E. (2021). Olfactory learning and memory in the greater short-nosed fruit bat Cynopterus sphinx: the influence of conspecifics distress calls, Journal of Comparative physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 207(5), 667-679. https://doi.org/10.1007/s00359-021-01505-2.
Rashidi S.K., Kalirad A., Rafie S., Behzad E. & Dezfouli M.A. (2023). The role of microRNAs in neurobiology and pathophysiology of the hippocampus, Front. Mol. Neurosci., 16, 1226413. https://doi.org/10.3389/fnmol.2023.1226413.
Said-Sadier, N., Sayegh, B., Farah, R., Abbas, L.A., Dweik, R., Tang, N. & Ojcius, D.M. (2023). Association between Periodontal Disease and Cognitive Impairment in Adults, Int. J. Environ. Res. Public Health, 20(6), 4707. https://doi.org/10.3390/ijerph20064707.
Sansores-España, L.D., Melgar-Rodríguez, S., Olivares-Sagredo, K., Cafferata, E.A., Martínez-Aguilar, V.M., Vernal, R., Paula-Lima, A.C. & Díaz-Zúñiga J. (2021). Oral-Gut-Brain Axis in Experimental Models of Periodontitis: Associating Gut Dysbiosis with Neurodegenerative Diseases, Front. Aging, 2, 781582. https://doi.org/10.3389/fragi.2021.781582.
Schütze, S., Döpke, A., Kellert, B., Seele, J., Ballüer, M., Bunkowski, S., Kreutzfeldt, M., Brück, W. & Nau, R. (2022). Intracerebral Infection with E. coli Impairs Spatial Learning and Induces Necrosis of Hippocampal Neurons in the Tg2576 Mouse Model of Alzheimer’s Disease, J. Alzheimer’s Dis. Rep., 6(1), 101-114. https://doi.org/10.3233/ADR-210049.
Shahbazi A., Sepehrinezhad A., Vahdani E., Jamali R., Ghasempour M., Massoudian S., Negah S.S. & Larsen F.S. (2023). Gut Dysbiosis and Blood-Brain Barrier Alteration in Hepatic Encephalopathy: From Gut to Brain, Biomedicines, 11(5), 1272. https://doi.org/10.3390/biomedicines11051272.
Squarzanti D.F., Dell’Atti F., Scalia A.C., Najmi Z., Cochis A. & Malfa P. (2024). Exploring the In Vitro Antibacterial Potential of Specific Probiotic Strains against Oral Pathogens, Microorganisms, 12(3), 441. https://doi.org/10.3390/microorganisms12030441.
Thangaleela S., Shanmugapriya V., Mukilan M., Radhakrishnan K. & Rajan K.E. (2018). Alterations in MicroRNA-132/212 Expression Impairs Fear Memory in Goldfish Carassius auratus, Ann. Neurosci., 25(2), 90-97. https://doi.org/10.1159/000486842.
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How to Cite
Potential effect of Escherichia coli Shiga toxin metabolites in the induction of cognitive dysfunction and stress memory formation in naïve goldfish Carassius auratus. (2025). Journal of Applied and Natural Science, 17(1), 339-347. https://doi.org/10.31018/jans.v17i1.6271
