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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 37, 2020 - Issue 7
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Original Articles

The circadian disruption of night work alters gut microbiota consistent with elevated risk for future metabolic and gastrointestinal pathology

ORCID Icon, &
Pages 1067-1081 | Received 17 Feb 2020, Accepted 01 Jun 2020, Published online: 30 Jun 2020

References

  • Alhasson F, Das S, Seth R, Dattaroy D, Chandrashekaran V, Ryan CN, Chan LS, Testerman T, Burch J, Hofseth LJ, et al. 2017. Altered gut microbiome in a mouse model of Gulf War Illness causes neuroinflammation and intestinal injury via leaky gut and TLR4 activation. PLoS One. 12(3):e0172914. doi:10.1371/journal.pone.0172914. PMID: 28328972.
  • Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. 2011. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun. 25(3):397–407. doi:0.1016/j.bbi.2010.10.023. PMID: 21040780.
  • Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M. 2010. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun. 78(4):1509–1519. doi:10.1128/IAI.00862-09. PMID: 20145094.
  • Bangsgaard Bendtsen KM, Krych L, Sorensen DB, Pang W, Nielsen DS, Josefsen K, Hansen LH, Sørensen SJ, Hansen AK. 2012. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS One. 7(10):e46231. doi:10.1371/journal.pone.0046231. PMID: 23056268.
  • Bannon C, Davies PJ, Collett A, Warhurst G. 2009. Potentiation of flagellin responses in gut epithelial cells by interferon-gamma is associated with STAT-independent regulation of MyD88 expression. Biochem J. 423(1):119–128. doi:10.1042/BJ20090392. PMID: 19619129.
  • Benedict C, Vogel H, Jonas W, Woting A, Blaut M, Schürmann A, Cedernaes J. 2016. Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals. Mol Metab. 5(12):1175–1186. doi:10.1016/j.molmet.2016.10.003. PMID: 27900260.
  • Blatchford P, Stoklosinski H, Eady S, Wallace A, Butts C, Gearry R, Gibson G, Ansell J. 2017. Consumption of kiwifruit capsules increases Faecalibacterium prausnitzii abundance in functionally constipated individuals: A randomised controlled human trial. J Nutr Sci. 6:e52. doi:10.1017/jns.2017.52. PMID: 29152256.
  • Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG. 2013. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods. 10(1):57–59. doi:10.1038/nmeth.2276. PMID: 23202435.
  • Brahe LK, Le Chatelier E, Prifti E, Pons N, Kennedy S, Hansen T, Pedersen O, Astrup A, Ehrlich SD, Larsen LH. 2015. Specific gut microbiota features and metabolic markers in postmenopausal women with obesity. Nutr Diabetes. 5:e159. doi:10.1038/nutd.2015.9. PMID: 26075636.
  • Cain SW, Filtness AJ, Phillips CL, Anderson C. 2015. Enhanced preference for high-fat foods following a simulated night shift. Scand J Work Environ Health. 41(3):288–293. doi:10.5271/sjweh.3486. PMID: 25699635.
  • Chen P, Starkel P, Turner JR, Ho SB, Schnabl B. 2014. Dysbiosis-induced intestinal inflammation activates TNFRI and mediates alcoholic liver disease in mice. Hepatology. 61(3):883–894. doi:10.1002/hep.27489. PMID: 25251280.
  • Deaver JA, Eum SY, Toborek M. 2018. Circadian disruption changes gut microbiome taxa and functional gene composition. Front Microbiol. 9:737. doi:10.3389/fmicb.2018.00737. PMID: 29706947.
  • Duck LW, Walter MR, Novak J, Kelly D, Tomasi M, Cong Y, Elson CO. 2007. Isolation of flagellated bacteria implicated in Crohn’s disease. Inflamma Bowel Dis. 13(10):1191–1201. doi:10.1002/ibd.20237. PMID: 17712838.
  • Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 10(10):996–998. doi:10.1038/nmeth.2604. PMID: 23955772.
  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 27(16):2194–2200. doi:10.1093/bioinformatics/btr381. PMID: 21700674.
  • Enck P, Aziz Q, Barbara G, Farmer AD, Fukudo S, Mayer EA, Niesler B, Quigley EM, Rajilić-Stojanović M, Schemann M, et al. 2016. Irritable bowel syndrome. Nat Rev Dis Primers. 2:16014. doi:10.1038/nrdp.2016.14. PMID: 27159638.
  • Eppinga H, Sperna Weiland CJ, Thio HB, van der Woude CJ, Nijsten TE, Peppelenbosch MP, Konstantinov SR. 2016. Similar depletion of protective Faecalibacterium prausnitzii in psoriasis and inflammatory bowel disease, but not in Hidradenitis Suppurativa. J Crohn’s Colitis. 10(9):1067–1075. doi:10.1093/ecco-jcc/jjw070. PMID: 26971052.
  • Everard A, Lazarevic V, Gaia N, Johansson M, Ståhlman M, Backhed F, Delzenne NM, Schrenzel J, François P, Cani PD. 2014. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. Isme J. 8(10):2116–2130. doi:10.1038/ismej.2014.45. PMID: 24694712.
  • Fleissner CK, Huebel N, Abd El-Bary MM, Loh G, Klaus S, Blaut M. 2010. Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br J Nutr. 104(6):919–929. doi:10.1017/S0007114510001303. PMID: 20441670.
  • Fonken LK, Aubrecht TG, Meléndez-Fernández OH, Weil ZM, Nelson RJ. 2013. Dim Light at night disrupts molecular circadian rhythms and affects metabolism. J Biol Rhythms. 28(4):262–271. doi:10.1177/0748730413493862. PMID: 23929553.
  • Fonken LK, Workman JL, Walton JC, Weil ZM, Morris JS, Haim A, Nelson RJ. 2010. Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci U S A. 107(43):18664–18669. doi:10.1073/pnas.1008734107. PMID: 20937863.
  • Furet J, Kong L, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Doré J, Henegar C, et al. 2010. Differential adaption of human gut microbiota to bariatric surgery induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 59(12):3049–3057. doi:10.2337/db10-0253. PMID: 20876719.
  • Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, et al. 2013. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 504(7480):446–450. doi:10.1038/nature12721. PMID: 24226770.
  • Hänninen A, Toivonen R, Pöysti S, Belzer C, Plovier H, Ouwerkerk JP, Emani R, Cani PD, De Vos WM. 2018. Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice. Gut. 67(8):1445–1453. doi:10.1136/gutjnl-2017-314508. PMID: 29269438.
  • Haro C, Garcia-Carpintero S, Alcala-Diaz JF, Gomez-Delgado F, Delgado-Lista J, Perez-Martinez P, Rangel Zuñiga OA, Quintana-Navarro GM, Landa BB, Clemente JC, et al. 2016. The gut microbial community in metabolic syndrome patients is modified by diet. J Biochem. 27:27–31. doi:10.1016/j.jnutbio.2015.08.011. PMID: 26376027.
  • Huang W, Ramsey KM, Marcheva B, Bass J. 2011. Circadian rhythms, sleep, and metabolism. J Clin Invest. 121(6):2133–2141. doi:10.1172/JCI46043. PMID: 21633182.
  • Jeffery IB, O’Toole PW, Öhman L, Claesson MJ, Deane J, Quigley EM, Simrén M. 2012. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut. 61(7):997. doi:10.1136/gutjnl-2011-301501. PMID: 22180058.
  • Jermendery G, Nadas J, Hegyi I, Vasas I, Hidvegi T. 2012. Assessment of cardiometabolic risk among shift workers in Hungary. Health Qual Life Outcomes. 10:18. doi:10.1186/1477-7525-10-18. PMID: 22296806.
  • Jumpertz R, Le DS, Turnbaugh PJ, Trinidad C, Bogardus C, Gordon JI, Krakoff J. 2011. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr. 94(1):58–65. doi:10.3945/ajcn.110.010132. PMID: 21543530.
  • Kameyama K, Itoh K. 2014. Intestinal colonization by a Lachnospiraceae bacterium contributes to the development of diabetes in obese mice. Microbes Environ. 9(4):427–430. doi:10.1264/jsme2.ME14054. PMID: 25283478.
  • Knowles SR, Nelson EA, Palombo EA. 2008. Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Biol Psychol. 77(2):132–137. doi:10.1016/j.biopsycho.2007.09.010. PMID: 18023961.
  • Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, Pierre JF, Heneghan AF, Nadimpalli A, Hubert N, et al. 2015. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe. 17(5):681–689. doi:10.1016/j.chom.2015.03.006. PMID: 25891358.
  • Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. 2005. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA. 102(31):11070–11075. doi:10.1073/pnas.0504978102. PMID: 16033867.
  • Ley RE, Turnbaugh PJ, Klein S, Gordon JI. 2006. Microbial ecology: human gut microbes associated with obesity. Nature. 444(7122):1022–1023. doi:10.1038/4441022a. PMID: 17183309.
  • Liu W, Zhang J, Wu C, Cai S, Huang W, Chen J, Xi X, Liang Z, Hou Q, Zhou B, et al. 2016. Unique features of ethnic Mongolian gut microbiome revealed by metagenomic analysis. Sci Rep. 6:34826. doi:10.1038/srep34826. PMID: 27708392.
  • Lopez-Siles M, Khan TM, Duncan SH, Harmsen HJ, Garcia-Gil LJ, Flint HJ. 2012. Cultured representatives of two major phylogroups of human colonic Faecalibacterium prausnitzii can utilize pectin, uronic acids, and host-derived substrates for growth. Appl Environ Microbiol. 78(2):420–428. doi:10.1128/AEM.06858-11. PMID: 22101049.
  • Lopez-Siles M, Martinez-Medina M, Abellà C, Busquets D, Sabat-Mir M, Duncan SH, Aldeguer X, Flint HJ, Garcia-Gil LJ. 2015. Mucosa-associated Faecalibacterium prausnitzii phylotype richness is reduced in patients with inflammatory bowel disease. Appl Environ Microbiol. 81(21):7582–7592. doi:10.1128/AEM.02006-15. PMID: 26296733.
  • Lopez-Siles M, Martinez-Medina M, Surís-Valls R, Aldeguer X, Sabat-Mir M, Duncan SH, Flint HJ, Garcia-Gil LJ. 2016. Changes in the abundance of Faecalibacterium prausnitzii phylogroups I and II in the intestinal mucosa of inflammatory bowel disease and patients with colorectal cancer. Inflamm Bowel Dis. 22(1):28–41. doi:10.1097/MIB.0000000000000590. PMID: 26595550.
  • Magoč T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 27(21):2957–2963. doi:10.1093/bioinformatics/btr507. PMID: 21903629.
  • Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, von Bergen M, McCoy KD, Macpherson AJ, Danska JS. 2013. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 339(6123):1084–1088. doi:10.1126/science.1233521. PMID: 23328391.
  • Martinez I, Perdicaro DJ, Brown AW, Hammons S, Carden TJ, Carr TP, Eskridge KM, Walter J. 2013. Diet-induced alterations of host cholesterol metabolism are likely to affect the gut microbiota composition in hamsters. Appl Environ Microbiol. 79(2):516–524. doi:10.1128/AEM.03046-12. PMID: 23124234.
  • Mathis D, Benoist C. 2012. The influence of the microbiota on type-1 diabetes: on the threshold of a leap forward in our understanding. Immunol Rev. 245(1):239–249. doi:10.1111/j.1600-065X.2011.01084.x. PMID: 22168424.
  • Mattson MP, Allison DB, Fontana L, Harvie M, Longo VD, Malaisse WJ, Mosley M, Notterpek L, Ravussin E, Scheer F, et al. 2014. Meal frequency and timing in health and disease. Proc Natl Acad Sci USA. 111(47):16647–16653. doi:10.1073/pnas.1413965111. PMID: 25404320.
  • Mendoza J, Pévet P, Challet E. 2007. Circadian and photic regulation of clock and clock-controlled proteins in the suprachiasmatic nuclei of calorie-restricted mice. Eur J Neurosci. 5(12):3691–3701. doi:10.1111/j.1460-9568.2007.05626.x. PMID: 17610588.
  • Mohawk JA, Green CB, Takahashi JS. 2012. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci. 35:445–462. doi:10.1146/annurev-neuro-060909-153128. PMID: 22483041.
  • Morikawa Y, Nakagawa H, Miura K, Soyama Y, Ishizaki M, Kido T, Naruse Y, Suwazono Y, Nogawa K. 2005. Shift work and the risk of diabetes mellitus among Japanese male factory workers. Scand J Work Environ Health. 31(3):179–183. doi:10.5271/sjweh.867. PMID: 15999569.
  • Nakanishi Y, Sato T, Ohteki T. 2015. Commensal gram-positive bacteria initiates colitis by inducing monocyte/macrophage mobilization. Mucosal Immunol. 8(1):152–160. doi:10.1038/mi.2014.53. PMID: 24938744.
  • Parkar SG, Kalsbeek A, Cheeseman CF. 2019. Potential role for the gut microbiota in modulating host circadian rhythms and metabolic health. Microorganisms. 7(2):41. doi:10.3390/microorganisms7020041. PMID: 30709031.
  • Pietroiusti A, Neri A, Somma G, Iavicoli I, Bergamaschi A, Magrini A. 2010. Incidence of metabolic syndrome among night-shift healthcare workers. Occup Environ Med. 67(1):54–57. doi:10.1136/oem.2009.046797. PMID: 19737731.
  • Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH. 2010. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 105(11):2420–2428. doi:10.1038/ajg.2010.281. PMID: 20648002.
  • Poroyko VA, Carreras A, Khalyfa A, Khalyfa AA, Leone V, Peris E, Almendros I, Gileles-Hillel A, Qiao Z, Hubert N, et al. 2016. Chronic sleep disruption alters gut microbiota, induces systemic and adipose tissue inflammation and insulin resistance in mice. Sci Rep. 6:35405. doi:10.1038/srep35405. PMID: 27739530.
  • Portaluppi F, Smolensky MH, Touitou Y. 2010. Ethics and methods for biological rhythm research on animals and human beings. Chronobiol Int. 27:1911–1929. doi:10.3109/07420528.2010.516381. PMID: 20969531.
  • Rajilic-Stojanovic M, Biagi E, Heilig HG, Kajander K, Kekkonen RA, Tims S, de Vos WM. 2011. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology. 141(5):1792–1801. doi:10.1053/j.gastro.2011.07.043. PMID: 21820992.
  • Reynolds AC, Paterson JL, Ferguson SA, Stanley D, Wright KP, Dawson D. 2017. The shift work and health research agenda: considering changes in gut microbiota as a pathway linking shift work, sleep loss and circadian misalignment, and metabolic disease. Sleep Med Rev. 34:3–9. doi:10.1016/j.smrv.2016.06.009. PMID: 27568341.
  • Riviere A, Selak M, Lantin D, Leroy F, De Vuyst L. 2016. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol. 7:979. doi:10.3389/fmicb.2016.00979. PMID: 27446020.
  • Rosselot AE, Hong CI, Moore SR. 2016. Rhythm and bugs: circadian clocks, gut microbiota, and enteric infections. Curr Opin Gastroenterol. 32(1):7–11. doi:10.1097/MOG.0000000000000227. PMID: 26628099.
  • Saini C, Suter DM, Liani A, Gos P, Schibler U. 2011. The mammalian circadian timing system: synchronization of peripheral clocks. Cold Spring Harb Symp Quant Biol. 76:39–47. doi:10.1146/annurev-physiol-021909-135821. PMID: 20148687.
  • Salonen A, de Vos WM, Palva A. 2010. Gastrointestinal microbiota in irritable bowel syndrome: present state and perspectives. Microbiology. 156(11):3205–3215. doi:10.1099/mic.0.043257-0. PMID: 20705664.
  • Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, Hardt PD. 2010. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring). 18(1):190–195. doi:10.1038/oby.2009.167. PMID: 19498350.
  • Smolensky MH, Hermida RC, Reinberg A, Sackett-Lundeen L, Portaluppi F. 2016. Circadian disruption: new clinical perspective of disease pathology and basis for chronotherapeutic intervention. Chronobiol Int. 33(8):1101‐1119. doi:10.1080/07420528.2016.1184678. PMID: 27308960.
  • Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Doré J. 2009. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 15(8):1183–1189. doi:10.1002/ibd.20903. PMID: 19235886.
  • Spencer MD, Hamp TJ, Reid RW, Fischer LM, Zeisel SH, Fodor AA. 2011. Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology. 140(3):976–986. doi:10.1053/j.gastro.2010.11.049. PMID: 21129376.
  • Tang W, Yao X, Xia F, Yang M, Chen Z, Zhou B, Liu Q. 2018. Modulation of the gut microbiota in rats by hugan qingzhi tablets during the treatment of high-fat-diet-induced nonalcoholic fatty liver disease. Oxid Med Cell Longev. 2018:7261619. doi:10.1155/2018/7261619. PMID: 30671174.
  • Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, Abramson L, Katz MN, Korem T, Zmora N, et al. 2014. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 159(3):514–529. doi:10.1016/j.cell.2014.09.048. PMID: 25417104.
  • Van den Abbeele P, Belzer C, Goossens M, Kleerebezem M, De Vos WM, Thas O, De Weirdt R, Kerckhof FM, Van de Wiele T. 2013. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. Isme J. 7(5):949–961. doi:10.1038/ismej.2012.158. PMID: 23235287.
  • Violanti JM, Burchfiel CM, Hartley TA, Mnatsakanova A, Fekedulegn D, Andrew ME, Charles LE, Vila BJ. 2009. Atypical work hours and metabolic syndrome among police officers. Arch Environ Occup Health. 64(3):194–201. doi:10.1080/19338240903241259. PMID: 19864222.
  • Voigt RM, Forsyth CB, Green SJ, Mutlu E, Engen P, Vitaterna MH, Turek FW, Keshavarzian A. 2014. Circadian disorganization alters intestinal microbiota. PLoS One. 9(5):e97500. doi:10.1371/journal.pone.0097500. PMID: 24848969.
  • Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 73(16):5261–5267. doi:10.1128/AEM.00062-07. PMID:17586664
  • Yang J, McDowell A, Kim EK, Seo H, Lee WH, Moon CM, Kym SM, Lee DH, Park YS, Jee YK, et al. 2019. Development of a colorectal cancer diagnostic model and dietary risk assessment through gut microbiome analysis. Exp Mol Med. 51:117. doi:10.1038/s12276-019-0313-4. PMID: 31582724.
  • Yurkovetskiy L, Burrows M, Khan AA, Graham L, Volchkov P, Becker L, Antonopoulos D, Umesaki Y, Chervonsky AV. 2013. Gender bias in autoimmunity is influenced by microbiota. Immunity. 39(2):400–412. doi:10.1016/j.immuni.2013.08.013. PMID: 23973225.
  • Zarrinpar A, Chaix A, Yooseph S, Panda S. 2014. Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab. 20(6):1006–1017. doi:10.1016/j.cmet.2014.11.008. PMID: 25470548.
  • Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, Mao Y, Zhang X, Pang X, Wei C, et al. 2010. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. Isme J. 4(2):232–241. doi:10.1038/ismej.2009.112. PMID: 19865183.
  • Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, et al. 2009. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA. 106(7):2365–2370. doi:10.1073/pnas.0812600106. PMID: 19164560.

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