Phylogenetic and metabolic tracking of gut microbiota during perinatal development

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Del Chierico, Federica ^a   Vernocchi, Pamela ^a,b   Petrucca, Andrea ^a,c   Paci, Paola ^d   Fuentes, Susana ^e   Praticò, Giulia ^f   Capuani, Giorgio ^f   Masotti, Andrea ^a   Reddel, Sofia ^a   Russo, Alessandra ^a   Vallone, Cristina ^g   Salvatori, Guglielmo ^a   Buffone, Elsa ^g   Signore, Fabrizio ^g   Rigon, Giuliano ^g   Dotta, Andrea ^a   Miccheli, Alfredo ^f   De Vos, Willem M ^e,h   Dallapiccola, Bruno ^a   Putignani, Lorenza ^a  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d CNR   (Italy)

^e WAGENINGEN UNIVERSITY   (Netherlands)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

^g SAN CAMILLO FORLANINI HOSPITAL   (Italy)

^h UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CESAREAN SECTION; COHORT ANALYSIS; CONTROLLED STUDY; FECES ANALYSIS; FEMALE; HOST; HUMAN; INFANT; INFANT FEEDING; INTESTINE FLORA; LACTATION; MALE; MECONIUM; METABOLITE; METABOLOME; MICROARRAY ANALYSIS; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROBIAL METABOLISM; MILK; NEWBORN; PERINATAL DEVELOPMENT; PERINATAL PERIOD; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; PROTON NUCLEAR MAGNETIC RESONANCE; VAGINAL DELIVERY; INTESTINE; MICROBIOLOGY; MICROFLORA; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

HUMANS; INFANT, NEWBORN; INTESTINES; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIOTA; PHYLOGENY;

EID: 84947475253     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137347     Document Type: Article

References (89)

1. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ Can Med Assoc J J Assoc Medicale Can. 2013; 185: 385-394. doi: 10.1503/cmaj.121189
2. Del Chierico F, Vernocchi P, Bonizzi L, Carsetti R, Castellazzi AM, Dallapiccola B, et al. Early-life gut microbiota under physiological and pathological conditions: the central role of combined meta-omicsbased approaches. J Proteomics. 2012; 75: 4580-4587. doi: 10.1016/j.jprot.2012.02.018 PMID: 22387117
3. Guarner F, Malagelada J-R. Gut flora in health and disease. Lancet. 2003; 361: 512-519. doi: 10.1016/S0140-6736(03)12489-0 PMID: 12583961
4. Jost T, Lacroix C, Braegger CP, Chassard C. New insights in gut microbiota establishment in healthy breast fed neonates. PloS One. 2012; 7: e44595. doi: 10.1371/journal.pone.0044595 PMID: 22957008
5. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio C-W, Santacruz N, et al. Peripheral education of the immune system by colonic commensal microbiota. Nature. 2011; 478: 250-254. doi: 10.1038/nature10434 PMID: 21937990
6. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009; 461: 1282-1286. doi: 10.1038/nature08530 PMID: 19865172
7. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012; 489: 231-241. doi: 10.1038/nature11551 PMID: 22972296
8. Sekirov I, Russell SL, Antunes LCM, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010; 90: 859-904. doi: 10.1152/physrev.00045.2009 PMID: 20664075
9. Young VB. The intestinal microbiota in health and disease. Curr Opin Gastroenterol. 2012; 28: 63-69. doi: 10.1097/MOG.0b013e32834d61e9 PMID: 22080827
10. Putignani L, Del Chierico F, Petrucca A, Vernocchi P, Dallapiccola B. The human gut microbiota: a dynamic interplay with the host from birth to senescence settled during childhood. Pediatr Res. 2014; 76: 2-10. doi: 10.1038/pr.2014.49 PMID: 24732106
11. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012; 489: 220-230. doi: 10.1038/nature11550 PMID: 22972295
12. Mondot S, de Wouters T, Doré J, Lepage P. The human gut microbiome and its dysfunctions. Dig Dis Basel Switz. 2013; 31: 278-285. doi: 10.1159/000354678
13. Pfefferle PI, Renz H. The mucosal microbiome in shaping health and disease. F1000prime Rep. 2014; 6: 11. doi: 10.12703/P6-11 PMID: 24592323
14. Relman DA. The human microbiome: ecosystem resilience and health. Nutr Rev. 2012; 70 Suppl 1: S2-9. doi: 10.1111/j.1753-4887.2012.00489.x PMID: 22861804
15. Fouhy F, Ross RP, Fitzgerald GF, Stanton C, Cotter PD. Composition of the early intestinal microbiota: knowledge, knowledge gaps and the use of high-throughput sequencing to address these gaps. Gut Microbes. 2012; 3: 203-220. doi: 10.4161/gmic.20169 PMID: 22572829
16. Gosalbes MJ, Llop S, Vallès Y, Moya A, Ballester F, Francino MP. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2013; 43: 198-211. doi: 10.1111/cea.12063
17. Madan JC, Farzan SF, Hibberd PL, Karagas MR. Normal neonatal microbiome variation in relation to environmental factors, infection and allergy. Curr Opin Pediatr. 2012; 24: 753-759. doi: 10.1097/MOP. 0b013e32835a1ac8 PMID: 23111681
18. Vallès Y, Artacho A, Pascual-García A, Ferrús ML, Gosalbes MJ, Abellán JJ, et al. Microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of Spanish infants. PLoS Genet. 2014; 10: e1004406. doi: 10.1371/journal.pgen.1004406 PMID: 24901968
19. Avershina E, Storrø O, Øien T, Johnsen R, Pope P, Rudi K. Major faecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiol Ecol. 2014; 87: 280-290. doi: 10.1111/1574-6941.12223 PMID: 24112053
20. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. 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: 11971-11975. doi: 10.1073/pnas.1002601107 PMID: 20566857
21. Fallani M, Young D, Scott J, Norin E, Amarri S, Adam R, et al. Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J Pediatr Gastroenterol Nutr. 2010; 51: 77-84. doi: 10.1097/MPG.0b013e3181d1b11e PMID: 20479681
22. Favier CF, de Vos WM, Akkermans ADL. Development of bacterial and bifidobacterial communities in feces of newborn babies. Anaerobe. 2003; 9: 219-229. doi: 10.1016/j.anaerobe.2003.07.001 PMID: 16887708
23. Gueimonde M, Sakata S, Kalliomäki M, Isolauri E, Benno Y, Salminen S. Effect of maternal consumption of lactobacillus GG on transfer and establishment of fecal bifidobacterial microbiota in neonates. J Pediatr Gastroenterol Nutr. 2006; 42: 166-170. doi: 10.1097/01.mpg.0000189346.25172.fd PMID: 16456409
24. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014; 63: 559-566. doi: 10.1136/gutjnl-2012-303249 PMID: 23926244
25. Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H, Francino MP. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol. 2010; 2: 53-66. doi: 10.1093/gbe/evp057 PMID: 20333224
26. LaTuga MS, Ellis JC, Cotton CM, Goldberg RN, Wynn JL, Jackson RB, et al. Beyond bacteria: a study of the enteric microbial consortium in extremely low birth weight infants. PloS One. 2011; 6: e27858. doi: 10.1371/journal.pone.0027858 PMID: 22174751
27. Mshvildadze M, Neu J, Shuster J, Theriaque D, Li N, Mai V. Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. J Pediatr. 2010; 156: 20-25. doi: 10.1016/j.jpeds. 2009.06.063 PMID: 19783002
28. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A. 2011; 108 Suppl 1: 4578-4585. doi: 10.1073/pnas.1000081107 PMID: 20668239
29. Moles L, Gómez M, Heilig H, Bustos G, Fuentes S, de Vos W, et al. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PloS One. 2013; 8: e66986. doi: 10.1371/journal.pone.0066986 PMID: 23840569
30. Jia W, Li H, Zhao L, Nicholson JK. Gut microbiota: a potential new territory for drug targeting. Nat Rev Drug Discov. 2008; 7: 123-129. doi: 10.1038/nrd2505 PMID: 18239669
31. Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014; 510: 417-421. doi: 10.1038/nature13421 PMID: 24896187
32. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007; 449: 804-810. doi: 10.1038/nature06244 PMID: 17943116
33. Zaneveld J, Turnbaugh PJ, Lozupone C, Ley RE, Hamady M, Gordon JI, et al. Host-bacterial coevolution and the search for new drug targets. Curr Opin Chem Biol. 2008; 12: 109-114. doi: 10.1016/j.cbpa. 2008.01.015 PMID: 18280814
34. Greiner T, Bäckhed F. Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab TEM. 2011; 22: 117-123. doi: 10.1016/j.tem.2011.01.002 PMID: 21353592
35. Nauta AJ, Ben Amor K, Knol J, Garssen J, van der Beek EM. Relevance of pre- and postnatal nutrition to development and interplay between the microbiota and metabolic and immune systems. Am J Clin Nutr. 2013; 98: 586S-93S. doi: 10.3945/ajcn.112.039644 PMID: 23824726
36. Nyangale EP, Mottram DS, Gibson GR. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J Proteome Res. 2012; 11: 5573-5585. doi: 10.1021/pr300637d PMID: 23116228
37. Chassard C, Lacroix C. Carbohydrates and the human gut microbiota. Curr Opin Clin Nutr Metab Care. 2013; 16: 453-460. doi: 10.1097/MCO.0b013e3283619e63 PMID: 23719143
38. Chassard C, de Wouters T, Lacroix C. Probiotics tailored to the infant: a window of opportunity. Curr Opin Biotechnol. 2014; 26: 141-147. doi: 10.1016/j.copbio.2013.12.012 PMID: 24469588
39. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012; 336: 1262-1267. doi: 10.1126/science.1223813 PMID: 22674330
40. Le Gall G, Noor SO, Ridgway K, Scovell L, Jamieson C, Johnson IT, et al. Metabolomics of fecal extracts detects altered metabolic activity of gut microbiota in ulcerative colitis and irritable bowel syndrome. J Proteome Res. 2011; 10: 4208-4218. doi: 10.1021/pr2003598 PMID: 21761941
41. Marchesi JR, Holmes E, Khan F, Kochhar S, Scanlan P, Shanahan F, et al. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res. 2007; 6: 546-551. doi: 10.1021/pr060470d PMID: 17269711
42. Pettersson J, Karlsson PC, Choi YH, Verpoorte R, Rafter JJ, Bohlin L. NMR metabolomic analysis of fecal water from subjects on a vegetarian diet. Biol Pharm Bull. 2008; 31: 1192-1198. PMID: 18520053
43. Chow J, Panasevich MR, Alexander D, Vester Boler BM, Rossoni Serao MC, Faber TA, et al. Fecal metabolomics of healthy breast-fed versus formula-fed infants before and during in vitro batch culture fermentation. J Proteome Res. 2014; 13: 2534-2542. doi: 10.1021/pr500011w PMID: 24628373
44. Sellitto M, Bai G, Serena G, Fricke WF, Sturgeon C, Gajer P, et al. Proof of concept of microbiomemetabolome analysis and delayed gluten exposure on celiac disease autoimmunity in genetically atrisk infants. PloS One. 2012; 7: e33387. doi: 10.1371/journal.pone.0033387 PMID: 22432018
45. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5: e177. doi: 10.1371/journal.pbio.0050177 PMID: 17594176
46. Jiménez E, Fernández L, Marín ML, Martín R, Odriozola JM, Nueno-Palop C, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol. 2005; 51: 270-274. doi: 10.1007/s00284-005-0020-3 PMID: 16187156
47. Adlerberth I, Wold AE. Establishment of the gut microbiota in Western infants. Acta Paediatr Oslo Nor 1992. 2009; 98: 229-238. doi: 10.1111/j.1651-2227.2008.01060.x
48. Khodayar-Pardo P, Mira-Pascual L, Collado MC, Martínez-Costa C. Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J Perinatol Off J Calif Perinat Assoc. 2014; 34: 599-605. doi: 10.1038/jp.2014.47
49. Joseph H. Connell. Mechanisms of Succession in Natural Communities and Their Role in Community Stability and Organization.
50. Connell Joseph H., Slatyer Ralph O. Mechanims of Succession in Natural communities and Their Role in Community Stability and Organization. The American Naturalist. 1977 111: 1119-1144.
51. Magne F, Abély M, Boyer F, Morville P, Pochart P, Suau A. Low species diversity and high interindividual variability in faeces of preterm infants as revealed by sequences of 16S rRNA genes and PCREarly temporal temperature gradient gel electrophoresis profiles. FEMS Microbiol Ecol. 2006; 57: 128-138. doi: 10.1111/j.1574-6941.2006.00097.x PMID: 16819956
52. Favier CF, Vaughan EE, De Vos WM, Akkermans ADL. Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol. 2002; 68: 219-226. PMID: 11772630
53. Jacquot A, Neveu D, Aujoulat F, Mercier G, Marchandin H, Jumas-Bilak E, et al. Dynamics and clinical evolution of bacterial gut microflora in extremely premature patients. J Pediatr. 2011; 158: 390-396. doi: 10.1016/j.jpeds.2010.09.007 PMID: 20961563
54. Schwiertz A, Gruhl B, Löbnitz M, Michel P, Radke M, Blaut M. Development of the intestinal bacterial composition in hospitalized preterm infants in comparison with breast-fed, full-term infants. Pediatr Res. 2003; 54: 393-399. doi: 10.1203/01.PDR.0000078274.74607.7A PMID: 12788986
55. Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am. 2013; 60: 49-74. doi: 10.1016/j.pcl.2012.10.002 PMID: 23178060
56. Duggan Christopher G, Watkins JB, Walker WA. Nutrition in pediatrics: basic science, clinical application. 4th ed. Hamilton: BC Decker; 2008.
57. Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977; 31: 107-133. doi: 10.1146/annurev.mi.31.100177.000543 PMID: 334036
58. Savage DC. Associations and physiological interactions of indigenous microorganisms and gastrointestinal epithelia. Am J Clin Nutr. 1972; 25: 1372-1379. PMID: 4565354
59. Chisholm RA, Pacala SW. Niche and neutral models predict asymptotically equivalent species abundance distributions in high-diversity ecological communities. Proc Natl Acad Sci U S A. 2010; 107: 15821-15825. doi: 10.1073/pnas.1009387107 PMID: 20733073
60. Jeraldo P, Sipos M, Chia N, Brulc JM, Dhillon AS, Konkel ME, et al. Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes. Proc Natl Acad Sci U S A. 2012; 109: 9692-9698. doi: 10.1073/pnas.1206721109 PMID: 22615407
61. Martínez I, Muller CE, Walter J. Long-term temporal analysis of the human fecal microbiota revealed a stable core of dominant bacterial species. PloS One. 2013; 8: e69621. doi: 10.1371/journal.pone. 0069621 PMID: 23874976
62. Matthews TJ, Whittaker RJ. Neutral theory and the species abundance distribution: recent developments and prospects for unifying niche and neutral perspectives. Ecol Evol. 2014; 4: 2263-2277. doi: 10.1002/ece3.1092 PMID: 25360266
63. Stecher B, Hardt W-D. Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol. 2011; 14: 82-91. doi: 10.1016/j.mib.2010.10.003 PMID: 21036098
64. Walter J, Ley R. The human gut microbiome: ecology and recent evolutionary changes. Annu Rev Microbiol. 2011; 65: 411-429. doi: 10.1146/annurev-micro-090110-102830 PMID: 21682646
65. He Y, Liu S, Leone S, Newburg DS. Human colostrum oligosaccharides modulate major immunologic pathways of immature human intestine. Mucosal Immunol. 2014; 7: 1326-1339. doi: 10.1038/mi.2014. 20 PMID: 24691111
66. Benno Y, Suzuki K, Suzuki K, Narisawa K, Bruce WR, Mitsuoka T. Comparison of the fecal microflora in rural Japanese and urban Canadians. Microbiol Immunol. 1986; 30: 521-532. PMID: 3747865
67. Park H-K, Shim S-S, Kim S-Y, Park J-H, Park S-E, Kim H-J, et al. Molecular analysis of colonized bacteria in a human newborn infant gut. J Microbiol Seoul Korea. 2005; 43: 345-353.
68. Catassi C, Bonucci A, Coppa GV, Carlucci A, Giorgi PL. Intestinal permeability changes during the first month: effect of natural versus artificial feeding. J Pediatr Gastroenterol Nutr. 1995; 21: 383-386. PMID: 8583288
69. Marcobal A, Barboza M, Froehlich JW, Block DE, German JB, Lebrilla CB, et al. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem. 2010; 58: 5334-5340. doi: 10.1021/jf9044205 PMID: 20394371
70. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol. 2007; 73: 1073-1078. doi: 10.1128/AEM.02340-06 PMID: 17189447
71. Macfarlane GT, Cummings JP. The colonic flora, fermentation and large bowel digestive function. The large intestine Physiology, pathophysiology and disease. Raven Press. New York: Shorter RG; 1991. pp. 51-92.
72. Rasmussen HS, Holtug K, Mortensen PB. Degradation of amino acids to short-chain fatty acids in humans. An in vitro study. Scand J Gastroenterol. 1988; 23: 178-182. PMID: 3363290
73. Jahan-Mihan A, Luhovyy BL, El Khoury D, Anderson GH. Dietary proteins as determinants of metabolic and physiologic functions of the gastrointestinal tract. Nutrients. 2011; 3: 574-603. doi: 10.3390/nu3050574 PMID: 22254112
74. Macfarlane GT, Macfarlane S. Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand J Gastroenterol Suppl. 1997; 222: 3-9. PMID: 9145437
75. Davila A-M, Blachier F, Gotteland M, Andriamihaja M, Benetti P-H, Sanz Y, et al. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. Pharmacol Res Off J Ital Pharmacol Soc. 2013; 68: 95-107. doi: 10.1016/j.phrs.2012.11.005
76. Miller TL, Wolin MJ. Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol. 1996; 62: 1589-1592. PMID: 8633856
77. Matschiavelli N, Oelgeschläger E, Cocchiararo B, Finke J, Rother M. Function and regulation of isoforms of carbon monoxide dehydrogenase/acetyl coenzyme A synthase in Methanosarcina acetivorans. J Bacteriol. 2012; 194: 5377-5387. doi: 10.1128/JB.00881-12 PMID: 22865842
78. Ragsdale SW. Metals and their scaffolds to promote difficult enzymatic reactions. Chem Rev. 2006; 106: 3317-3337. doi: 10.1021/cr0503153 PMID: 16895330
79. Lindahl PA. Nickel-carbon bonds in acetyl-coenzyme a synthases/carbon monoxide dehydrogenases. Met Ions Life Sci. 2009; 6: 133-150. doi: 10.1039/BK9781847559159-00133 PMID: 20877794
80. Salonen A, Nikkilä J, Jalanka-Tuovinen J, Immonen O, Rajilić-Stojanović M, Kekkonen RA, et al. Comparative analysis of fecal of mice. J Nutr. 2013; 143: 1549-1557. doi: 10.3945/jn.113.177105
81. Rajilić-Stojanović M, Heilig HGHJ, Molenaar D, Kajander K, Surakka A, Smidt H, et al. Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ Microbiol. 2009; 11: 1736-1751. doi: 10.1111/j.1462-2920.2009.01900.x PMID: 19508560
82. Tan PK, Downey TJ, Spitznagel EL Jr, Xu P, Fu D, Dimitrov DS, et al. Evaluation of gene expression measurements from commercial microarray platforms. Nucleic Acids Res. 2003; 31: 5676-5684. PMID: 14500831
83. Jalanka-Tuovinen J, Salonen A, Nikkilä J, Immonen O, Kekkonen R, Lahti L, et al. Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PloS One. 2011; 6: e23035. doi: 10.1371/journal.pone.0023035 PMID: 21829582
84. Lahti L, Elo LL, Aittokallio T, Kaski S. Probabilistic analysis of probe reliability in differential gene expression studies with short oligonucleotide arrays. IEEEACM Trans Comput Biol Bioinforma IEEE ACM. 2011; 8: 217-225. doi: 10.1109/TCBB.2009.38
85. Brasili E, Mengheri E, Tomassini A, Capuani G, Roselli M, Finamore A, et al. Lactobacillus acidophilus La5 and Bifidobacterium lactis Bb12 induce different age-related metabolic profiles revealed by 1HNMR spectroscopy in urine and feces of mice. J Nutr. 2013; 143: 1549-1557. doi: 10.3945/jn.113. 177105 PMID: 23946343
86. Saric J, Wang Y, Li J, Coen M, Utzinger J, Marchesi JR, et al. Species variation in the fecal metabolome gives insight into differential gastrointestinal function. J Proteome Res. 2008; 7: 352-360. doi: 10.1021/pr070340k PMID: 18052033
87. Jacobs DM, Deltimple N, van Velzen E, van Dorsten FA, Bingham M, Vaughan EE, et al. (1)H NMR metabolite profiling of feces as a tool to assess the impact of nutrition on the human microbiome. NMR Biomed. 2008; 21: 615-626. doi: 10.1002/nbm.1233 PMID: 18085514
88. Wishart DS, Jewison T, Guo AC, Wilson M, Knox C, Liu Y, et al. HMDB 3.0-The Human Metabolome Database in 2013. Nucleic Acids Res. 2013; 41: D801-807. doi: 10.1093/nar/gks1065 PMID: 23161693
89. Jackson JE. A user's guide to principal components. New York [u.a.]: Wiley; 1991.