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http://dx.doi.org/10.4196/kjpp.2021.25.6.575

Aging effects on the diurnal patterns of gut microbial composition in male and female mice  

Kim, Hyun-Jung (Department of Pharmacology, College of Medicine, Ewha Womans University)
Moon, Chang Mo (Department of Internal Medicine, College of Medicine, Ewha Womans University)
Kang, Jihee Lee (Inflammation-Cancer Microenvironment Research Center, College of Medicine, Ewha Womans University)
Park, Eun-Mi (Department of Pharmacology, College of Medicine, Ewha Womans University)
Publication Information
The Korean Journal of Physiology and Pharmacology / v.25, no.6, 2021 , pp. 575-583 More about this Journal
Abstract
Composition of the gut microbiota changes with aging and plays an important role in age-associated disease such as metabolic syndrome, cancer, and neurodegeneration. The gut microbiota composition oscillates through the day, and the disruption of their diurnal rhythm results in gut dysbiosis leading to metabolic and immune dysfunctions. It is well documented that circadian rhythm changes with age in several biological functions such as sleep, body temperature, and hormone secretion. However, it is not defined whether the diurnal pattern of gut microbial composition is affected by aging. To evaluate aging effects on the diurnal pattern of the gut microbiome, we evaluated the taxa profiles of cecal contents obtained from young and aged mice of both sexes at daytime and nighttime points by 16S rRNA gene sequencing. At the phylum level, the ratio of Firmicutes to Bacteroidetes and the relative abundances of Verrucomicrobia and Cyanobacteria were increased in aged male mice at night compared with that of young male mice. Meanwhile, the relative abundances of Sutterellaceae, Alloprevotella, Lachnospiraceae UCG-001, and Parasutterella increased in aged female mice at night compared with that of young female mice. The Lachnospiraceae NK4A136 group relative abundance increased in aged mice of both sexes but at opposite time points. These results showed the changes in diurnal patterns of gut microbial composition with aging, which varied depending on the sex of the host. We suggest that disturbed diurnal patterns of the gut microbiome can be a factor for the underlying mechanism of age-associated gut dysbiosis.
Keywords
Aging; Diurnal rhythm; Dysbiosis; Gut microbiota; Sex difference;
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1 Spychala MS, Venna VR, Jandzinski M, Doran SJ, Durgan DJ, Ganesh BP, Ajami NJ, Putluri N, Graf J, Bryan RM, McCullough LD. Age-related changes in the gut microbiota influence systemic inflammation and stroke outcome. Ann Neurol. 2018;84:23-36.   DOI
2 Shao X, Sun C, Tang X, Zhang X, Han D, Liang S, Qu R, Hui X, Shan Y, Hu L, Fang H, Zhang H, Wu X, Chen C. Anti-inflammatory and intestinal microbiota modulation properties of Jinxiang garlic (Allium sativum L.) polysaccharides toward dextran sodium sulfate-induced colitis. J Agric Food Chem. 2020;68:12295-12309.   DOI
3 Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, von Bergen M, McCoy KD, Macpherson AJ, Danska JS. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 2013;339:1084-1088.   DOI
4 Yurkovetskiy L, Burrows M, Khan AA, Graham L, Volchkov P, Becker L, Antonopoulos D, Umesaki Y, Chervonsky AV. Gender bias in autoimmunity is influenced by microbiota. Immunity. 2013;39:400-412.   DOI
5 Razavi AC, Potts KS, Kelly TN, Bazzano LA. Sex, gut microbiome, and cardiovascular disease risk. Biol Sex Differ. 2019;10:29.   DOI
6 Cuervo-Zanatta D, Garcia-Mena J, Perez-Cruz C. Gut microbiota alterations and cognitive impairment are sexually dissociated in a transgenic mice model of Alzheimer's disease. J Alzheimers Dis. 2021;82(s1):S195-S214.   DOI
7 Buford TW. (Dis)Trust your gut: the gut microbiome in age-related inflammation, health, and disease. Microbiome. 2017;5:80.   DOI
8 Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, Bianchetti A, Volta GD, Turla M, Cotelli MS, Gennuso M, Prelle A, Zanetti O, Lussignoli G, Mirabile D, Bellandi D, et al. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging. 2017;49:60-68.   DOI
9 Bishehsari F, Voigt RM, Keshavarzian A. Circadian rhythms and the gut microbiota: from the metabolic syndrome to cancer. Nat Rev Endocrinol. 2020;16:731-739.   DOI
10 Rehman T. Role of the gut microbiota in age-related chronic inflammation. Endocr Metab Immune Disord Drug Targets. 2012;12:361-367.   DOI
11 DeJong EN, Surette MG, Bowdish DME. The gut microbiota and unhealthy aging: disentangling cause from consequence. Cell Host Microbe. 2020;28:180-189.   DOI
12 Burcelin R, Serino M, Chabo C, Blasco-Baque V, Amar J. Gut microbiota and diabetes: from pathogenesis to therapeutic perspective. Acta Diabetol. 2011;48:257-273.   DOI
13 Banks G, Nolan PM, Peirson SN. Reciprocal interactions between circadian clocks and aging. Mamm Genome. 2016;27:332-340.   DOI
14 Thaiss CA, Levy M, Korem T, Dohnalova L, Shapiro H, Jaitin DA, David E, Winter DR, Gury-BenAri M, Tatirovsky E, Tuganbaev T, Federici S, Zmora N, Zeevi D, Dori-Bachash M, Pevsner-Fischer M, Kartvelishvily E, Brandis A, Harmelin A, Shibolet O, et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell. 2016;167:1495-1510.e12.   DOI
15 Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, Sitaraman SV, Knight R, Ley RE, Gewirtz AT. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science. 2010;328:228-231.   DOI
16 Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027-1031.   DOI
17 Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R, Turroni S, Consolandi C, Quercia S, Scurti M, Monti D, Capri M, Brigidi P, Candela M. Gut microbiota and extreme longevity. Curr Biol. 2016;26:1480-1485.   DOI
18 Karlsson FH, Fak F, Nookaew I, Tremaroli V, Fagerberg B, Petranovic D, Backhed F, Nielsen J. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245.   DOI
19 Keshavarzian A, Green SJ, Engen PA, Voigt RM, Naqib A, Forsyth CB, Mutlu E, Shannon KM. Colonic bacterial composition in Parkinson's disease. Mov Disord. 2015;30:1351-1360.   DOI
20 Mohawk JA, Green CB, Takahashi JS. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci. 2012;35:445-462.   DOI
21 Nakamura TJ, Nakamura W, Yamazaki S, Kudo T, Cutler T, Colwell CS, Block GD. Age-related decline in circadian output. J Neurosci. 2011;31:10201-10205.   DOI
22 Zarrinpar A, Chaix A, Yooseph S, Panda S. Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab. 2014;20:1006-1017.   DOI
23 Schmalle V, Lorentz A. Role of the microbiota in circadian rhythms of the host. Chronobiol Int. 2020;37:301-310.   DOI
24 Kim KA, Jeong JJ, Yoo SY, Kim DH. Gut microbiota lipopolysaccharide accelerates inflamm-aging in mice. BMC Microbiol. 2016;16:9.   DOI
25 Hoffman JD, Parikh I, Green SJ, Chlipala G, Mohney RP, Keaton M, Bauer B, Hartz AMS, Lin AL. Age drives distortion of brain metabolic, vascular and cognitive functions, and the gut microbiome. Front Aging Neurosci. 2017;9:298.   DOI
26 Insenser M, Murri M, Del Campo R, Martinez-Garcia MA, Fernandez-Duran E, Escobar-Morreale HF. Gut microbiota and the polycystic ovary syndrome: influence of sex, sex hormones, and obesity. J Clin Endocrinol Metab. 2018;103:2552-2562.   DOI
27 Liang X, Bushman FD, FitzGerald GA. Rhythmicity of the intestinal microbiota is regulated by gender and the host circadian clock. Proc Natl Acad Sci U S A. 2015;112:10479-10484.   DOI
28 Wang J, Feng W, Zhang S, Chen L, Tang F, Sheng Y, Ao H, Peng C. Gut microbial modulation in the treatment of chemotherapy-induced diarrhea with Shenzhu Capsule. BMC Complement Altern Med. 2019;19:126.   DOI
29 Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, Abramson L, Katz MN, Korem T, Zmora N, Kuperman Y, Biton I, Gilad S, Harmelin A, Shapiro H, Halpern Z, Segal E, Elinav E. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 2014;159:514-529.   DOI
30 Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, Pierre JF, Heneghan AF, Nadimpalli A, Hubert N, Zale E, Wang Y, Huang Y, Theriault B, Dinner AR, Musch MW, Kudsk KA, Prendergast BJ, Gilbert JA, Chang EB. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe. 2015;17:681-689.   DOI
31 Shin JA, Jeong SI, Kim M, Yoon JC, Kim HS, Park EM. Visceral adipose tissue inflammation is associated with age-related brain changes and ischemic brain damage in aged mice. Brain Behav Immun. 2015;50:221-231.   DOI
32 Jeong SI, Shin JA, Cho S, Kim HW, Lee JY, Kang JL, Park EM. Resveratrol attenuates peripheral and brain inflammation and reduces ischemic brain injury in aged female mice. Neurobiol Aging. 2016;44:74-84.   DOI
33 Crespo-Piazuelo D, Estelle J, Revilla M, Criado-Mesas L, RamayoCaldas Y, Ovilo C, Fernandez AI, Ballester M, Folch JM. Characterization of bacterial microbiota compositions along the intestinal tract in pigs and their interactions and functions. Sci Rep. 2018;8:12727.   DOI
34 Park SH, Kim KA, Ahn YT, Jeong JJ, Huh CS, Kim DH. Comparative analysis of gut microbiota in elderly people of urbanized towns and longevity villages. BMC Microbiol. 2015;15:49.   DOI
35 Lee SM, Kim N, Yoon H, Kim YS, Choi SI, Park JH, Lee DH. Compositional and functional changes in the gut microbiota in irritable bowel syndrome patients. Gut Liver. 2021;15:253-261.   DOI
36 Yoon CH, Ryu JS, Moon J, Kim MK. Association between aging-dependent gut microbiome dysbiosis and dry eye severity in C57BL/6 male mouse model: a pilot study. BMC Microbiol. 2021;21:106.   DOI
37 Lin CH, Chen CC, Chiang HL, Liou JM, Chang CM, Lu TP, Chuang EY, Tai YC, Cheng C, Lin HY, Wu MS. Altered gut microbiota and inflammatory cytokine responses in patients with Parkinson's disease. J Neuroinflammation. 2019;16:129.   DOI
38 Langille MG, Meehan CJ, Koenig JE, Dhanani AS, Rose RA, Howlett SE, Beiko RG. Microbial shifts in the aging mouse gut. Microbiome. 2014;2:50.   DOI
39 Chen Q, Wu J, Dong X, Yin H, Shi X, Su S, Che B, Li Y, Yang J. Gut flora-targeted photobiomodulation therapy improves senile dementia in an Aß-induced Alzheimer's disease animal model. J Photochem Photobiol B. 2021;216:112152.   DOI
40 Liu Y, Li T, Alim A, Ren D, Zhao Y, Yang X. Regulatory effects of stachyose on colonic and hepatic inflammation, gut microbiota dysbiosis, and peripheral CD4+ T cell distribution abnormality in highfat diet-fed mice. J Agric Food Chem. 2019;67:11665-11674.   DOI
41 Wang CS, Li WB, Wang HY, Ma YM, Zhao XH, Yang H, Qian JM, Li JN. VSL#3 can prevent ulcerative colitis-associated carcinogenesis in mice. World J Gastroenterol. 2018;24:4254-4262.   DOI
42 Smolensky MH, Portaluppi F, Manfredini R, Hermida RC, Tiseo R, Sackett-Lundeen LL, Haus EL. Diurnal and twenty-four hour patterning of human diseases: acute and chronic common and uncommon medical conditions. Sleep Med Rev. 2015;21:12-22.   DOI
43 Chen YJ, Wu H, Wu SD, Lu N, Wang YT, Liu HN, Dong L, Liu TT, Shen XZ. Parasutterella, in association with irritable bowel syndrome and intestinal chronic inflammation. J Gastroenterol Hepatol. 2018;33:1844-1852.   DOI
44 Kiely CJ, Pavli P, O'Brien CL. The microbiome of translocated bacterial populations in patients with and without inflammatory bowel disease. Intern Med J. 2018;48:1346-1354.   DOI
45 Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, Hammer RE, Williams SC, Crowley J, Yanagisawa M, Gordon JI. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A. 2008;105:16767-16772.   DOI
46 Tu MY, Han KY, Chang GR, Lai GD, Chang KY, Chen CF, Lai JC, Lai CY, Chen HL, Chen CM. Kefir peptides prevent estrogen deficiency-induced bone loss and modulate the structure of the gut microbiota in ovariectomized mice. Nutrients. 2020;12:3432.   DOI