Modulation of gut microbiota by dietary supplementation with tuna oil and algae oil alleviates the effects of D-galactose-induced ageing
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Previous studies have shown that dietary supplementation with tuna oil and algae oil can alleviate the effects of ageing on learning and memory in mouse models, but the mechanism of this effect remains unknown. This study aimed to determine whether dietary oil supplementation alters the composition of the gut microbiota during the prevention of age-related effects on cognition. Ageing mice received dietary oil supplementation continuously for 12 weeks. The supplementation was found to improve the animals’ learning and cognition, and this effect was most marked in the TO200AO400 group, which received a 1:2 mixture of tuna oil and algae oil at 600 mg kg−1 day−1. Next-generation sequencing of the 16S rRNA gene present in faecal samples showed that the gut microbiota varied in the groups that received different oil treatments; the TO200AO400 treatment most closely restored the composition of the D-galactose-altered gut microbiota to that of the control. Moreover, 83 altered operational taxonomic units (OTUs) responsive to dietary oil supplementation were identified; five of these differed in one or more parameters associated with host ageing. In conclusion, this study confirmed the effect of dietary oil supplementation on the alleviation of age-related decline in cognitive function and showed that oil supplementation results in alterations in the composition of the gut microbiota. Further research will be needed to elucidate the causal relationship between the reversal of age-related cognitive decline and gut microbiota modulation and to explore the potential of gut microbial communities as a diagnostic biomarker and a therapeutic target in ageing.
KeywordsAgeing Tuna oil Algae oil Mixture Gut microbiota
We thank Nature Research Editing Service for English language editing.
This work was supported by the Regional Demonstration Project of Marine Economic Innovation and Development in 2014 and 2016, the Natural Science Foundation of Zhejiang Province (Y18C010005), the Open Research Fund of Key Laboratory of Animal Protein Food Processing Technology of Zhejiang Province and the K.C. Wong Magna Fund in Ningbo University.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All experimental procedures and animal care were performed in accordance with the Guide for the Care and Use of Laboratory Animals prepared by the Ningbo University Laboratory Animal Center (affiliated with the Zhejiang Laboratory Animal Common Service Platform), and all the animal protocols were approved by the Ningbo University Laboratory Animal Center under permit number No. SYXK (ZHE 2008-0110).
- Ait-Belgnaoui A, Colom A, Braniste V, Ramalho L, Marrot A, Cartier C, Houdeau E, Theodorou V, Tompkins T (2014) Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroent Motil 26(4):510–520. https://doi.org/10.1111/nmo.12295 CrossRefGoogle Scholar
- Campbell EL, Macmanus CF, Kominsky DJ, Keely S, Glover LE, Bowers BE, Scully M, Bruyninckx WJ, Colgan SP (2010) Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. P Natl Acad Sci USA 107(32):14298–14303. https://doi.org/10.1073/pnas.0914730107 CrossRefGoogle Scholar
- Carvalho C, Machado N, Mota PC, Correia SC, Cardoso S, Santos RX, Santos MS, Oliveira CR, Moreira PI (2013) Type 2 diabetic and Alzheimer’s disease mice present similar behavioral, cognitive, and vascular anomalies. J Alzheimers Dis 35(3):623–635. https://doi.org/10.3233/JAD-130005 PubMedGoogle Scholar
- Chen ZH, Saito Y, Yoshida Y, Sekine A, Noguchi N, Niki E (2005) 4-Hydroxynonenal induces adaptive response and enhances PC12 cell tolerance primarily through induction of thioredoxin reductase 1 via activation of Nrf2. J Biol Chem 280(51):41921–41927. https://doi.org/10.1074/jbc.M508556200 CrossRefPubMedGoogle Scholar
- Cui X, Zuo P, Zhang Q, Li X, Hu Y, Long J, Packer L, Liu J (2006) Chronic systemic D-galactose exposure induces memory loss, neurodegeneration, and oxidative damage in mice: protective effects of R-alpha-lipoic acid. J Neurosci Res 84(3):647–654. https://doi.org/10.1002/jnr.20899 CrossRefPubMedGoogle Scholar
- Dasilva G, Pazos M, García-Egido E, Pérez-Jiménez J, Torres JL, Giralt M, Nogués MR, Medina I (2016) Lipidomics to analyze the influence of diets with different EPA:DHA ratios in the progression of metabolic syndrome using SHROB rats as a model. Food Chem 205:196–203. https://doi.org/10.1016/j.foodchem.2016.03.020 CrossRefPubMedGoogle Scholar
- Freund LY, Vedin I, Cederholm T, Basun H, Faxén IG, Eriksdotter M, Hjorth E, Schultzberg M, Vessby B, Wahlund LO (2014) Transfer of omega-3 fatty acids across the blood-brain barrier after dietary supplementation with a docosahexaenoic acid-rich omega-3 fatty acid preparation in patients with Alzheimer’s disease: the OmegAD study. J Intern Med 275(4):428–436. https://doi.org/10.1111/joim.12166 CrossRefGoogle Scholar
- Giudice MMD, Indolfi C, Capasso M, Maiello N, Decimo F, Ciprandi G (2017) Bifidobacterium mixture (B longum BB536, B infantis M-63, B breve M-16V) treatment in children with seasonal allergic rhinitis and intermittent asthma. Ital Journal Pediatr 43(1):25. https://doi.org/10.1186/s13052-017-0340-5 CrossRefGoogle Scholar
- Grant WB (2016) Reducing the risk of Alzheimer’s disease: NSAIDs, fish oils, and diet. BMJ 327(747):128Google Scholar
- Lanctôt KL, Herrmann N, Mazzotta P, Khan LR, Ingber N (2004) GABAergic function in Alzheimer’s disease: evidence for dysfunction and potential as a therapeutic target for the treatment of behavioural and psychological symptoms of dementia. Can J Psychiatr 49(7):439–453. https://doi.org/10.1177/070674370404900705 CrossRefGoogle Scholar
- Liang CY, Liang YM, Liu HZ, Zhu DM, Hou SZ, Wu YY, Huang S, Lai XP (2017) Effect of Dendrobium officinale on D-galactose-induced aging mice. Chin J Integr Med. https://doi.org/10.1007/s11655-016-2631-x
- Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin R, O’Hara R (2013) Vegan: community ecology package version 2.0-10. Lorenzo Cachón Rodríguez 48(9):103–132Google Scholar
- Patel NV, Gordon MN, Connor KE, Good RA, Engelman RW, Mason J, Morgan DG, Morgan TE, Finch CE (2005) Caloric restriction attenuates Aβ-deposition in Alzheimer transgenic models. Neurobiol Aging 26(7):995–1000. https://doi.org/10.1016/j.neurobiolaging.2004.09.014 CrossRefPubMedGoogle Scholar
- Pierpaola D, Tijana M, Andrea C, Angela L, Domenico DA (2016) ROS, cell senescence, and novel molecular mechanisms in aging and age-related diseases. Oxidative Med Cell Longev 2016(1):3565127Google Scholar
- Riahi Y, Cohen G, Shamni O, Sasson S (2010) Signaling and cytotoxic functions of 4-hydroxyalkenals. Am J Physiol-Endoc M 299(6):E879–E886Google Scholar
- Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. https://doi.org/10.1128/AEM.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
- Solfrizzi V, Colacicco AM, D'Introno A, Capurso C, Torres F, Rizzo C, Capurso A, Panza F (2006) Dietary intake of unsaturated fatty acids and age-related cognitive decline: a 8.5-year follow-up of the Italian longitudinal study on aging. Neurobiol Aging 27(11):1694–1704. https://doi.org/10.1016/j.neurobiolaging.2005.09.026 CrossRefPubMedGoogle Scholar
- Su KP, Lai HC, Yang HT, Su WP, Peng CY, Chang JP, Chang HC, Pariante CM (2014) Omega-3 fatty acids in the prevention of interferon-alpha-induced depression: results from a randomized, controlled trial. Biol Psychiatry 76(7):559–566. https://doi.org/10.1016/j.biopsych.2014.01.008 CrossRefPubMedGoogle Scholar
- Yu Y, Bai F, Wang W, Liu Y, Yuan Q, Qu S, Zhang T, Tian G, Li S, Li D (2015) Fibroblast growth factor 21 protects mouse brain against D-galactose induced aging via suppression of oxidative stress response and advanced glycation end products formation. Pharmacol Biochem Be 133(1):122–131. https://doi.org/10.1016/j.pbb.2015.03.020 CrossRefGoogle Scholar
- Zhang Q, Huang Y, Li X, Cui X, Zuo P, Li J (2005) GM1 ganglioside prevented the decline of hippocampal neurogenesis associated with D-galactose. Neuroreport 16(12):1297–1301. https://doi.org/10.1097/01.wnr.0000174405.24763.bc CrossRefPubMedGoogle Scholar