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Intermittent fasting supports the balance of the gut microbiota composition

Abstract

There is a growing body of detailed research demonstrating that intermittent fasting is essentially a cleansing activity in terms of health. Especially since its applications that exceed 16 h trigger autophagy, it continues its effect on all tissue and organ systems after the regeneration movement that starts at the cellular level. Similarly, it continues to be better understood with each passing day that the gut microbiota (GM) has many positive effects on all tissue and organ systems. Although the GM is affected by many different parameters, dietary habits are reported to be the most effective factor. Therefore, it is important to investigate the effects of different preferred fasting practices on the GM, which has numerous health benefits. Pointing out this situation, this study aims to determine the effects of 18-h intermittent fasting for 5 weeks on the shaping of GM. A 12-month-old male Wistar rat was chosen as the model organism in the study. At the end of the application, the metagenome was applied to the cecum content of the intestinal tissue collected from the sacrificed animals. Intermittent fasting practice led to an increase in alpha diversity, which expresses a significant bacterial diversity, the stabilization of Firmicutes and Bacteroidetes ratios (F/B), and the reshaping of the values with the highest prevalence in all stages of the classification, especially in the family, genus, and species care. Analysis results showed that the preferred intermittent fasting program helps balance the GM composition. This study is an important example showing the strong positive link between intermittent fasting and GM.

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Data availability

All data generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

There is not any custom computer code or algorithm used to generate the results reported in the manuscript.

References

  • Ai D, Pan H, Li X, Gao Y, Liu G, Xia LC (2019) Identifying gut microbiota associated with colorectal cancer using a zero-inflated lognormal model. Front Microbiol 10:826

    PubMed  PubMed Central  Article  Google Scholar 

  • Ali I, Liu K, Long D, Faisal S, Hilal MG, Ali I, Huang X, Long R (2021) Ramadan fasting leads to shifts in human gut microbiota structured by dietary composition. Front Microbiol. https://doi.org/10.3389/fmicb.2021.642999

    Article  PubMed  PubMed Central  Google Scholar 

  • Arias L, Goig GA, Cardona P, Torres-Puente M, Díaz J, Rosales Y, Garcia E, Tapia G, Comas I, Vilaplana C, Cardona PJ (2019) Influence of gut microbiota on progression to tuberculosis generated by high fat diet-induced obesity in C3HeB/FeJ mice. Front Immunol 10:1–18

    Article  CAS  Google Scholar 

  • Boutard M, Cerisy T, Nogue P-Y, Alberti A, Weissenbach J, Salanoubat M, Tolonen AC (2014) Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. PLoS Genet 10:e1004773

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Cani PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67:1716–1725

    CAS  PubMed  Article  Google Scholar 

  • Cenit MC, Sanz Y, Codoñer-Franch P (2017) Influence of gut microbiota on neuropsychiatric disorders. World J Gastroenterol 23:5486–5498

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ceylani T, Jakubowska-Doğru E, Gurbanov R, Teker HT, Gozen AG (2018) The effects of repeated antibiotic administration to juvenile BALB/c mice on the microbiota status and animal behavior at the adult age. Heliyon 4:e00644

    PubMed  PubMed Central  Article  Google Scholar 

  • Ceylani T, Taner H, Samgane G, Gurbanov R (2022) Intermittent fasting-induced biomolecular modifications in rat tissues detected by ATR-FTIR spectroscopy and machine learning algorithms. Anal Biochem 654:114825

    CAS  PubMed  Article  Google Scholar 

  • Chang D-H, Rhee M-S, Ahn S, Bang B-H, Oh JE, Lee HK, Kim B-C (2015) Faecalibaculum rodentium gen. nov., sp. nov., isolated from the faeces of a laboratory mouse. Antonie Van Leeuwenhoek 108:1309–1318

    CAS  PubMed  Article  Google Scholar 

  • Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:260–270

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cho D-Y, Skinner D, Lim DJ, Mclemore JG, Koch CG, Zhang S, Swords WE, Hunter R, Crossman DK, Crowley MR, Grayson JW, Rowe SM, Woodworth BA (2020) The impact of Lactococcus lactis (probiotic nasal rinse) co-culture on growth of patient-derived strains of Pseudomonas aeruginosa. Int Forum Allergy Rhinol 10:444–449

    PubMed  PubMed Central  Article  Google Scholar 

  • Cignarella F, Cantoni C, Ghezzi L, Salter A, Dorsett Y, Chen L, Phillips D, Weinstock GM, Fontana L, Cross AH, Zhou Y, Piccio L (2018) Intermittent fasting confers protection in CNS autoimmunity by altering the gut microbiota. Cell Metab 27:1222-1235.e6

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cresci GA, Bawden E (2015) Gut microbiome: what we do and don’t know. Nutr Clin Pract off Publ Am Soc Parenter Enter Nutr 30:734–746

    CAS  Google Scholar 

  • Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701–712

    CAS  PubMed  Article  Google Scholar 

  • de Cabo R, Mattson MP (2019) Effects of intermittent fasting on health, aging, and disease. N Engl J Med 381:2541–2551

    PubMed  Article  Google Scholar 

  • Fan Y, Pedersen O (2021) Gut microbiota in human metabolic health and disease. Nat Rev Microbiol 19:55–71

    CAS  PubMed  Article  Google Scholar 

  • Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9:577–589

    CAS  PubMed  Article  Google Scholar 

  • Fraumene C, Manghina V, Cadoni E, Marongiu F, Abbondio M, Serra M, Palomba A, Tanca A, Laconi E, Uzzau S (2018) Caloric restriction promotes rapid expansion and long-lasting increase of Lactobacillus in the rat fecal microbiota. Gut Microbes 9:104–114

    PubMed  Article  Google Scholar 

  • Gianchecchi E, Fierabracci A (2019) Recent advances on microbiota involvement in the pathogenesis of autoimmunity. Int J Mol Sci. https://doi.org/10.3390/ijms20020283

    Article  PubMed  PubMed Central  Google Scholar 

  • Gurbanov R, Kabaoğlu U, Yağcı T (2022) Metagenomic analysis of intestinal microbiota in wild rats living in urban and rural habitats. Folia Microbiol (praha) 67:469–477

    CAS  Article  Google Scholar 

  • Haas JT, Staels B (2017) Fasting the microbiota to improve metabolism? Cell Metab 26:584–585

    CAS  PubMed  Article  Google Scholar 

  • Heiman ML, Greenway FL (2016) A healthy gastrointestinal microbiome is dependent on dietary diversity. Mol Metab 5:317–320

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Hugerth LW, Andreasson A, Talley NJ, Forsberg AM, Kjellström L, Schmidt PT, Agreus L, Engstrand L (2020) No distinct microbiome signature of irritable bowel syndrome found in a Swedish random population. Gut 69:1076–1084

    PubMed  Article  Google Scholar 

  • Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

  • Jain N, Walker WA (2015) Diet and host-microbial crosstalk in postnatal intestinal immune homeostasis. Nat Rev Gastroenterol Hepatol 12:14–25

    CAS  PubMed  Article  Google Scholar 

  • Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, Björkstén B, Engstrand L, Andersson AF (2014) Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63:559–566

    CAS  PubMed  Article  Google Scholar 

  • Kalamaki MS, Angelidis AS (2020) High-throughput, sequence-based analysis of the microbiota of Greek Kefir grains from two geographic regions. Food Technol Biotechnol 58:138–146

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kim S, Jazwinski SM (2018) The gut microbiota and healthy aging: a mini-review. Gerontology 64:513–520

    CAS  PubMed  Article  Google Scholar 

  • Klement R, Pazienza V (2019) Impact of different types of diet on gut microbiota profiles and cancer prevention and treatment. Medicina (b Aires) 55:84

    Article  Google Scholar 

  • Li G, Xie C, Lu S, Nichols RG, Tian Y, Li L, Patel D, Ma Y, Brocker CN, Yan T, Krausz KW, Xiang R, Gavrilova O, Patterson AD, Gonzalez FJ (2017) Intermittent fasting promotes white adipose browning and decreases obesity by shaping the gut microbiota. Cell Metab 26:672-685.e4

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Li Q, Hu W, Liu W-X, Zhao L-Y, Huang D, Liu X-D, Chan H, Zhang Y, Zeng J-D, Coker OO, Kang W, Ng SSM, Zhang L, Wong SH, Gin T, Chan MTV, Wu J-L, Yu J, Wu WKK (2021) Streptococcus thermophilus inhibits colorectal tumorigenesis through secreting β-galactosidase. Gastroenterology 160:1179-1193.e14

    CAS  PubMed  Article  Google Scholar 

  • Liu Z, Dai X, Zhang H, Shi R, Hui Y, Jin X, Zhang W, Wang L, Wang Q, Wang D, Wang J, Tan X, Ren B, Liu X, Zhao T, Wang J, Pan J, Yuan T, Chu C, Lan L, Yin F, Cadenas E, Shi L, Zhao S, Liu X (2020) Gut microbiota mediates intermittent-fasting alleviation of diabetes-induced cognitive impairment. Nat Commun. https://doi.org/10.1038/s41467-020-14676-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch SV, Pedersen O (2016) The Human Intestinal Microbiome in Health and Disease. N Engl J Med 375:2369–2379

    CAS  PubMed  Article  Google Scholar 

  • Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, Balamurugan R (2020) The firmicutes/bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients. https://doi.org/10.3390/nu12051474

    Article  PubMed  PubMed Central  Google Scholar 

  • Matthews JA (2014) Diversity Indices. Encycl Environ Chang 1–7

  • Mattson MP, Longo VD, Harvie M (2017) Impact of intermittent fasting on health and disease processes. Ageing Res Rev 39:46–58

    PubMed  Article  Google Scholar 

  • Meehan CJ, Beiko RG (2014) A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 6:703–713

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • O’Toole PW, Jeffery IB (2015) Gut microbiota and aging. Science 350:1214–1215

    PubMed  Article  CAS  Google Scholar 

  • Paoli A, Tinsley G, Bianco A, Moro T (2019) The influence of meal frequency and timing on health in humans: The role of fasting. Nutrients. https://doi.org/10.3390/nu11040719

    Article  PubMed  PubMed Central  Google Scholar 

  • Petersen C, Round JL (2014) Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol 16:1024–1033

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto J-M, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Quigley EMM (2017) Microbiota-brain-gut axis and neurodegenerative diseases. Curr Neurol Neurosci Rep. https://doi.org/10.1007/s11910-017-0802-6

    Article  PubMed  Google Scholar 

  • Razavi AC, Potts KS, Kelly TN, Bazzano LA (2019) Sex, gut microbiome, and cardiovascular disease risk. Biol Sex Differ 10:29

    PubMed  PubMed Central  Article  Google Scholar 

  • Rodríguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N, Avershina E, Rudi K, Narbad A, Jenmalm MC, Marchesi JR, Collado MC (2015) The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis 26:26050

    PubMed  Google Scholar 

  • Shafquat A, Joice R, Simmons SL, Huttenhower C (2014) Functional and phylogenetic assembly of microbial communities in the human microbiome. Trends Microbiol 22:261–266

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Silva YP, Bernardi A, Frozza RL (2020) The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front Endocrinol (lausanne) 11:25

    Article  Google Scholar 

  • Singh R, Lakhanpal D, Kumar S, Sharma S, Kataria H, Kaur M, Kaur G (2012) Late-onset intermittent fasting dietary restriction as a potential intervention to retard age-associated brain function impairments in male rats. Age (dordr) 34:917–933

    CAS  Article  Google Scholar 

  • Singh R, Manchanda S, Kaur T, Kumar S, Lakhanpal D, Lakhman SS, Kaur G (2015) Middle age onset short-term intermittent fasting dietary restriction prevents brain function impairments in male Wistar rats. Biogerontology 16:775–788

    CAS  PubMed  Article  Google Scholar 

  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031

    PubMed  Article  Google Scholar 

  • Vasconcelos AR, Yshii LM, Viel TA, Buck HS, Mattson MP, Scavone C, Kawamoto EM (2014) Intermittent fasting attenuates lipopolysaccharide-induced neuroinflammation and memory impairment. J Neuroinflammation 11:85

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Wood DE, Salzberg SL (2014) Kraken: Ultrafast metagenomic sequence classification using exact alignments. Genome Biol. https://doi.org/10.1186/gb-2014-15-3-r46

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, Zadeh M, Gong M, Qi Y, Zubcevic J, Sahay B, Pepine CJ, Raizada MK, Mohamadzadeh M (2015) Gut dysbiosis is linked to hypertension. Hypertension 65:1331–1340

    CAS  PubMed  Article  Google Scholar 

  • Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zagato E, Pozzi C, Bertocchi A, Schioppa T, Saccheri F, Guglietta S, Fosso B, Melocchi L, Nizzoli G, Troisi J, Marzano M, Oresta B, Spadoni I, Atarashi K, Carloni S, Arioli S, Fornasa G, Asnicar F, Segata N, Guglielmetti S, Honda K, Pesole G, Vermi W, Penna G, Rescigno M (2020) Endogenous murine microbiota member Faecalibaculum rodentium and its human homologue protect from intestinal tumour growth. Nat Microbiol 5:511–524

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zarrinpar A, Chaix A, Yooseph S, Panda S (2014) Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab 20:1006–1017

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zhang J, Zhan Z, Li X, Xing A, Jiang C, Chen Y, Shi W, An L (2017) Intermittent fasting protects against Alzheimer’s disease possible through restoring aquaporin-4 polarity. Front Mol Neurosci 10:395

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zhang Y, Zhou S, Zhou Y, Yu L, Zhang L, Wang Y (2018) Altered gut microbiome composition in children with refractory epilepsy after ketogenic diet. Epilepsy Res 145:163–168

    PubMed  Article  Google Scholar 

  • Zheng X, Wang S, Jia W (2018) Calorie restriction and its impact on gut microbial composition and global metabolism. Front Med 12:634–644

    PubMed  Article  Google Scholar 

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All authors contributed to the conception and design of the study. The final manuscript has been read and approved by all authors. HTT and TC conducted animal experiments and supervised the study. TC and HTT analyzed the results and wrote the manuscript.

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Correspondence to Taha Ceylani.

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This study was carried out with the approval of the Ethics Committee (approval number: 2021/05) from the Saki Yenilli Experimental Animal Production and Practice Laboratory.

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Teker, H.T., Ceylani, T. Intermittent fasting supports the balance of the gut microbiota composition. Int Microbiol (2022). https://doi.org/10.1007/s10123-022-00272-7

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  • DOI: https://doi.org/10.1007/s10123-022-00272-7

Keywords

  • Intermittent fasting
  • Gut microbiota
  • Dysbiosis
  • Metagenomics
  • Alpha diversity
  • Wistar rat