Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort
Tóm tắt
The gut is the most extensively studied niche of the human microbiome. The aim of this study was to characterise the initial gut microbiota development of a cohort of breastfed infants (n = 192) from 1 to 24 weeks of age. V4-V5 region 16S rRNA amplicon Illumina sequencing and, in parallel, bacteriological culture. The metabolomic profile of infant urine at 4 weeks of age was also examined by LC-MS. Full-term (FT), spontaneous vaginally delivered (SVD) infants’ microbiota remained stable at both phylum and genus levels during the 24-week period examined. FT Caesarean section (CS) infants displayed an increased faecal abundance of Firmicutes (p < 0.01) and lower abundance of Actinobacteria (p < 0.001) after the first week of life compared to FT-SVD infants. FT-CS infants gradually progressed to harbouring a microbiota closely resembling FT-SVD (which remained stable) by week 8 of life, which was maintained at week 24. The gut microbiota of preterm (PT) infants displayed a significantly greater abundance of Proteobacteria compared to FT infants (p < 0.001) at week 1. Metabolomic analysis of urine at week 4 indicated PT-CS infants have a functionally different metabolite profile than FT (both CS and SVD) infants. Co-inertia analysis showed co-variation between the urine metabolome and the faecal microbiota of the infants. Tryptophan and tyrosine metabolic pathways, as well as fatty acid and bile acid metabolism, were found to be affected by delivery mode and gestational age. These findings confirm that mode of delivery and gestational age both have significant effects on early neonatal microbiota composition. There is also a significant difference between the metabolite profile of FT and PT infants. Prolonged breastfeeding was shown to have a significant effect on the microbiota composition of FT-CS infants at 24 weeks of age, but interestingly not on that of FT-SVD infants. Twins had more similar microbiota to one another than between two random infants, reflecting the influence of similarities in both host genetics and the environment on the microbiota.
Tài liệu tham khảo
Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012;489:231–41.
Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–7.
Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6:237ra65.
Cilieborg MS, Boye M, Sangild PT. Bacterial colonization and gut development in preterm neonates. Early Hum Dev. 2012. doi: 10.1016/j.earlhumdev.2011.12.027.
Dominguez-Bello CEK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107:11971–5.
Azad MB, Konya T, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL. Impact of cesarean section delivery and breastfeeding on infant gut microbiota at one year of age. Allergy Asthma Clin Immunol. 2014;10:A24.
Adlerberth I. Factors influencing the establishment of the intestinal microbiota in infancy. Nestle Nutr Work Ser Pediatr Progr. 2008;62:13–33.
Adlerberth I, Wold AE. Establishment of the gut microbiota in Western infants. Acta Paediatr. 2009;98:229–38.
Fanaro S, Chierici R, Guerrini P, Vigi V. Intestinal microflora in early infancy: composition and development. Acta Paediatr Suppl. 2003;91:48–55.
Hesla HM, Stenius F, Jäderlund L, Nelson R, Engstrand L, Alm J, Dicksved J. Impact of lifestyle on the gut microbiota of healthy infants and their mothers—the Aladdin birth cohort. FEMS Microbiol Ecol. 2014. doi: 10.1111/1574-6941.12434.
Hussey S, Wall R, Gruffman E, O’Sullivan L, Ryan CA, Murphy B, Fitzgerald G, Stanton C, Ross RP. Parenteral antibiotics reduce bifidobacteria colonization and diversity in neonates. Int J Microbiol. 2011. doi: 10.1155/2011/130574.
Bäckhed F, Roswall J, Peng Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690–703.
Tannock GW, Lawley B, Munro K, et al. Comparison of the compositions of the stool microbiotas of infants fed goat milk formula, cow milk-based formula, or breast milk. Appl Environ Microbiol. 2013;79:3040–8.
Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A. 2011;108(Suppl):4578–85.
La Rosa PS, Warner BB, Zhou Y, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci. 2014;111:12522–7.
Gale C, Logan KM, Santhakumaran S, Parkinson JRC, Hyde MJ, Modi N. Effect of breastfeeding compared with formula feeding on infant body composition: a systematic review and meta-analysis. Am J Clin Nutr. 2012;95:656–69.
Innis S. Human milk: maternal dietary lipids and infant development. Proc Nutr Soc. 2007;66:397–404.
Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5, e177.
Knol J, Scholtens P, Kafka C, Steenbakkers J, Gro S, Helm K, Klarczyk M, Schöpfer H, Böckler H-M, Wells J. Colon microflora in infants fed formula with galacto- and fructo-oligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr. 2005;40:36–42.
Stewart CJ, Marrs ECL, Nelson A, Lanyon C, Perry JD, Embleton ND, Cummings SP, Berrington JE. Development of the preterm gut microbiome in twins at risk of necrotising enterocolitis and sepsis. PLoS One. 2013;8, e73465.
Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA. Development of the preterm infant gut microbiome: a research priority. Microbiome. 2014;2:38.
Kamada N, Núñez G. Regulation of the immune system by the resident intestinal bacteria. Gastroenterology. 2014;146:1477–88.
Zeissig S, Blumberg RS. Life at the beginning: perturbation of the microbiota by antibiotics in early life and its role in health and disease. Nat Immunol. 2014;15:307–10.
Kamada N, Seo S-U, Chen GY, Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13:321–35.
Yu Z, Morrison M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques. 2004;36:808–12.
Fernández-Peralbo M, de Castro L. Preparation of urine samples prior to targeted or untargeted metabolomics mass-spectrometry analysis. doi: 10.1016/j.trac.2012.08.011.
Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–63.
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.
Benjamini Y, Hochberg J. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B. 1995;57:289–300.
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.
Claesson MJ, Jeffery IB, Conde S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488:178–84.
Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, Sears MR, Becker AB, Scott JA, Kozyrskyj AL. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185:385–94.
Avershina E, Storrø O, Øien T, Johnsen R, Wilson R, Egeland T, Rudi K. Bifidobacterial succession and correlation networks in a large unselected cohort of mothers and their children. Appl Environ Microbiol. 2013;79:497–507.
Dogra S, Sakwinska O, Soh S-E, et al. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. MBio. 2015;6:e02419–14.
Hyde MJ, Griffin JL, Herrera E, Byrne CD, Clarke L, Kemp PR. Delivery by Caesarean section, rather than vaginal delivery, promotes hepatic steatosis in piglets. Clin Sci. 2010;118:47–59.
Dessì A, Atzori L, Noto A, et al. Metabolomics in newborns with intrauterine growth retardation (IUGR): urine reveals markers of metabolic syndrome. J Matern Fetal Neonatal Med. 2011;24 Suppl 2:35–9.
Russell WR, Duncan SH, Scobbie L, Duncan G, Cantlay L, Calder AG, Anderson SE, Flint HJ. Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. Mol Nutr Food Res. 2013;57:523–35.
O’Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res. 2014;277:1–17.
Zheng P, Zeng B, Zhou C, et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism. Mol Psychiatry. 2016;21(6):786–96.
Strandvik B, Wahlén E, Wikström S-A. The urinary bile acid excretion in healthy premature and full-term infants during the neonatal period. Scand J Clin Lab Invest. 1994;54:1–10.
Yousef IM, Perwaiz S, Lamireau T, Tuchweber B. Urinary bile acid profile in children with inborn errors of bile acid metabolism and chronic cholestasis; screening technique using electrospray tandem mass-spectrometry (ES/MS/MS). Med Sci Monit. 2003;9:MT21–31.
Weuve J, Sánchez BN, Calafat AM, Schettler T, Green RA, Hu H, Hauser R. Exposure to phthalates in neonatal intensive care unit infants: urinary concentrations of monoesters and oxidative metabolites. Environ Health Perspect. 2006;114:1424–31.
Carlstedt F, Jönsson BAG, Bornehag C-G. PVC flooring is related to human uptake of phthalates in infants. Indoor Air. 2013;23:32–9.
Koeth RA, Wang Z, Levison BS, et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med. 2013;19:576–85.
Marcobal A, Barboza M, Sonnenburg ED, et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe. 2011;10:507–14.
Murphy K, O’ Shea CA, Ryan CA, Dempsey EM, O’ Toole PW, Stanton C, Ross RP. The gut microbiota composition in dichorionic triplet sets suggests a role for host genetic factors. PLoS One. 2015;10:e0122561.
Cox LM, Yamanishi S, Sohn J, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158:705–21.
van Nimwegen FA, Penders J, Stobberingh EE, et al. Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy. J Allergy Clin Immunol. 2011;128:948–55.e1–3.
Kerr CA, Grice DM, Tran CD, Bauer DC, Li D, Hendry P, Hannan GN. Early life events influence whole-of-life metabolic health via gut microflora and gut permeability. Crit Rev Microbiol. 2014. doi:10.3109/1040841X.2013.837863.
Rodríguez JM, Murphy K, Stanton C, et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015;26:26050.
Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–4.
Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science. 2012;336:1262–7.
Clarke G, O’Mahony SM, Dinan TG, Cryan JF. Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr. 2014;103:812–9.
Bezirtzoglou E, Tsiotsias A, Welling GW. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe. 2011;17:478–82.
Yamasaki C, Totsu S, Uchiyama A, Nakanishi H, Masumoto K, Washio Y, Shuri K, Ishida S, Imai K, Kusuda S. Effect of Bifidobacterium administration on very-low-birthweight infants. Pediatr Int. 2012;54:651–6.
Saez-Lara MJ, Gomez-Llorente C, Plaza-Diaz J, Gil A. The role of probiotic lactic acid bacteria and bifidobacteria in the prevention and treatment of inflammatory bowel disease and other related diseases: a systematic review of randomized human clinical trials. Biomed Res Int. 2015;2015:505878.
Picard C, Fioramonti J, Francois A, Robinson T, Neant F, Matuchansky C. Review article: bifidobacteria as probiotic agents—physiological effects and clinical benefits. Aliment Pharmacol Ther. 2005;22:495–512.
Solís G, de Los Reyes-Gavilan CG, Fernández N, Margolles A, Gueimonde M. Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe. 2010;16:307–10.
Ahrne S, Lonnermark E, Wold AE, Aberg N, Hesselmar B, Saalman R, Strannegard IL, Molin G, Adlerberth I. Lactobacilli in the intestinal microbiota of Swedish infants. Microbes Infect. 2005;7:1256–62.