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Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants


Although knowledge of the complex community of microbes that inhabits the human gut is constantly increasing, the successional process through which it develops during infancy remains poorly understood. Particularly, although gut microbiota composition is known to vary through time among infants, the effect of this variability on the functional capacities of the community has not been previously explored. We simultaneously analyze the taxonomic and functional development of the gut microbiota in a birth cohort of healthy infants during the first year of life, showing that individual instances of gut colonization vary in their temporal dynamics and that clear parallelisms exist between functional and taxonomic change. Therefore, taxonomic composition shapes the functional capacities of the microbiota, and, consequently, successional variability may affect host physiology, metabolism and immunity. Nevertheless, we detect some overarching trends in microbiota development, such as the existence of two distinct phases of succession, separated by the introduction of solid foods, and a strong directionality of change towards the taxonomic and functional composition of the maternal microbiota. Understanding the commonalities and differences among individual patterns of gut colonization in healthy infants will enable a better definition of the deviations in this process that result in microbiota imbalances and disease.


Vyšlo v časopise: Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004406
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004406

Souhrn

Although knowledge of the complex community of microbes that inhabits the human gut is constantly increasing, the successional process through which it develops during infancy remains poorly understood. Particularly, although gut microbiota composition is known to vary through time among infants, the effect of this variability on the functional capacities of the community has not been previously explored. We simultaneously analyze the taxonomic and functional development of the gut microbiota in a birth cohort of healthy infants during the first year of life, showing that individual instances of gut colonization vary in their temporal dynamics and that clear parallelisms exist between functional and taxonomic change. Therefore, taxonomic composition shapes the functional capacities of the microbiota, and, consequently, successional variability may affect host physiology, metabolism and immunity. Nevertheless, we detect some overarching trends in microbiota development, such as the existence of two distinct phases of succession, separated by the introduction of solid foods, and a strong directionality of change towards the taxonomic and functional composition of the maternal microbiota. Understanding the commonalities and differences among individual patterns of gut colonization in healthy infants will enable a better definition of the deviations in this process that result in microbiota imbalances and disease.


Zdroje

1. SekirovI, RussellSL, AntunesLC, FinlayBB (2010) Gut microbiota in health and disease. Physiol Rev 90: 859–904.

2. Collado MC, D'Auria G, Mira A, Francino MP (2013) Human Microbiome and Diseases: A Metagenomic Approach. In: Watson RR and Preedy VR, editors. Bioactive Food as Dietary Interventions for Liver and Gastrointestinal Disease. San Diego: Academic Press. pp. 235–249.

3. Baas-Becking L (1934) Geobiologie of inleiding tot de milieukunde. Van Stockum & Zoon. 263 p.

4. de WitR, BouvierT (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8: 755–758.

5. McConnellEL, BasitAW, MurdanS (2008) Measurements of rat and mouse gastrointestinal pH, fluid and lymphoid tissue, and implications for in-vivo experiments. J Pharm Pharmacol 60: 63–70.

6. PalmerC, BikEM, DiGiulioDB, RelmanDA, BrownPO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5: e177.

7. TurnbaughPJ, LeyRE, HamadyM, Fraser-LiggettCM, KnightR, et al. (2007) The human microbiome project. Nature 449: 804–810.

8. TurnbaughPJ, HamadyM, YatsunenkoT, CantarelBL, DuncanA, et al. (2009) A core gut microbiome in obese and lean twins. Nature 457: 480–484.

9. QinJ, LiR, RaesJ, ArumugamM, BurgdorfKS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59–65.

10. Jalanka-TuovinenJ, SalonenA, NikkilaJ, ImmonenO, KekkonenR, et al. (2011) Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS One 6: e23035.

11. ArumugamM, RaesJ, PelletierE, Le PaslierD, YamadaT, et al. (2011) Enterotypes of the human gut microbiome. Nature 473: 174–180.

12. KorenO, KnightsD, GonzalezA, WaldronL, SegataN, et al. (2013) A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol 9: e1002863.

13. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton, New Jersey, USA: Princeton University Press.

14. Gilpin M, editor(1991) Metapopulation Dynamics: Empirical and Theoretical Investigations. London: Academic Press.

15. HubbellSP (2006) Neutral theory and the evolution of ecological equivalence. Ecology 87: 1387–1398.

16. VaishampayanPA, KuehlJV, FroulaJL, MorganJL, OchmanH, et al. (2010) Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol 2: 53–66.

17. GosalbesMJ, DurbanA, PignatelliM, AbellanJJ, Jimenez-HernandezN, et al. (2011) Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS One 6: e17447.

18. VallesY, GosalbesMJ, de VriesLE, AbellanJJ, FrancinoMP (2012) Metagenomics and development of the gut microbiota in infants. Clin Microbiol Infect 18 Suppl 4: 21–26.

19. PetcheyOL, GastonKJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9: 741–758.

20. McGillBJ, EnquistBJ, WeiherE, WestobyM (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21: 178–185.

21. TringeSG, von MeringC, KobayashiA, SalamovAA, ChenK, et al. (2005) Comparative metagenomics of microbial communities. Science 308: 554–557.

22. GillSR, PopM, DeboyRT, EckburgPB, TurnbaughPJ, et al. (2006) Metagenomic analysis of the human distal gut microbiome. Science 312: 1355–1359.

23. KurokawaK, ItohT, KuwaharaT, OshimaK, TohH, et al. (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14: 169–181.

24. HMP Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486: 207–214.

25. YatsunenkoT, ReyFE, ManaryMJ, TrehanI, Dominguez-BelloMG, et al. (2012) Human gut microbiome viewed across age and geography. Nature 486: 222–227.

26. RautavaS, RuuskanenO, OuwehandA, SalminenS, IsolauriE (2004) The hygiene hypothesis of atopic disease–an extended version. J Pediatr Gastroenterol Nutr 38: 378–388.

27. NoverrMC, HuffnagleGB (2005) The ‘microflora hypothesis’ of allergic diseases. Clin Exp Allergy 35: 1511–1520.

28. PendersJ, StobberinghEE, van den BrandtPA, ThijsC (2007) The role of the intestinal microbiota in the development of atopic disorders. Allergy 62: 1223–1236.

29. Dominguez-BelloMG, CostelloEK, ContrerasM, MagrisM, HidalgoG, et al. (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107: 11971–11975.

30. MackieRI, SghirA, GaskinsHR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69: 1035S–1045S.

31. BiasucciG, BenenatiB, MorelliL, BessiE, BoehmG (2008) Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr 138: 1796S–1800S.

32. AzadMB, KonyaT, MaughanH, GuttmanDS, FieldCJ, et al. (2013) Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 185: 385–394.

33. AvershinaE, StorroO, OienT, JohnsenR, PopeP, et al. (2014) Major faecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiol Ecol 87: 280–290.

34. FavierCF, VaughanEE, De VosWM, AkkermansAD (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68: 219–226.

35. KoenigJE, SporA, ScalfoneN, FrickerAD, StombaughJ, et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108 Suppl 1: 4578–4585.

36. CapdevilaF, VizmanosB, Marti-HennebergC (1998) Implications of the weaning pattern on macronutrient intake, food volume and energy density in non-breastfed infants during the first year of life. J Am Coll Nutr 17: 256–262.

37. MarkowitzVM, ChenIM, ChuK, SzetoE, PalaniappanK, et al. (2012) IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Res 40: D123–129.

38. KorenO, GoodrichJK, CullenderTC, SporA, LaitinenK, et al. (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150: 470–480.

39. JimenezE, FernandezL, MarinML, MartinR, OdriozolaJM, et al. (2005) Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 51: 270–274.

40. JimenezE, MarinML, MartinR, OdriozolaJM, OlivaresM, et al. (2008) Is meconium from healthy newborns actually sterile? Res Microbiol 159: 187–193.

41. GosalbesMJ, LlopS, VallesY, MoyaA, BallesterF, et al. (2013) Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy 43: 198–211.

42. MshvildadzeM, NeuJ, ShusterJ, TheriaqueD, LiN, et al. (2010) Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. J Pediatr 156: 20–25.

43. MadanJC, SalariRC, SaxenaD, DavidsonL, O'TooleGA, et al. (2012) Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch Dis Child Fetal Neonatal Ed 97: F456–462.

44. MolesL, GomezM, HeiligH, BustosG, FuentesS, et al. (2013) Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One 8: e66986.

45. MorG, CardenasI (2010) The immune system in pregnancy: a unique complexity. Am J Reprod Immunol 63: 425–433.

46. NewbernD, FreemarkM (2011) Placental hormones and the control of maternal metabolism and fetal growth. Curr Opin Endocrinol Diabetes Obes 18: 409–416.

47. PerezPF, DoreJ, LeclercM, LevenezF, BenyacoubJ, et al. (2007) Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics 119: e724–732.

48. Donnet-HughesA, PerezPF, DoreJ, LeclercM, LevenezF, et al. (2010) Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nutr Soc 69: 407–415.

49. AmarJ, ChaboC, WagetA, KloppP, VachouxC, et al. (2011) Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Mol Med 3: 559–572.

50. Cabrera-RubioR, ColladoM, LaitinenK, SalminenS, IsolauriE, et al. (2012) The human milk microbiome changes over lactation and is shaped by maternal weight and mode delivery. Am J Clin Nutr 96: 544–551.

51. PendersJ, ThijsC, VinkC, StelmaFF, SnijdersB, et al. (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118: 511–521.

52. ConnellJH, SlatyerRO (1977) Mechanims of Succession in Natural Communities and Their Role in Community Stability and Organization. The American Naturalist 111: 1119–1144.

53. FiererN, NemergutD, KnightR, CraineJM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161: 635–642.

54. NgSK, HamiltonIR (1971) Lactate metabolism by Veillonella parvula. J Bacteriol 105: 999–1005.

55. RochaEP (2004) Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14: 2279–2286.

56. TamamesJ, AbellanJJ, PignatelliM, CamachoA, MoyaA (2010) Environmental distribution of prokaryotic taxa. BMC Microbiol 10: 85.

57. StarkPL, LeeA (1982) The bacterial colonization of the large bowel of pre-term low birth weight neonates. J Hyg (Lond) 89: 59–67.

58. KunzC, RudloffS, BaierW, KleinN, StrobelS (2000) Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 20: 699–722.

59. MarcobalA, BarbozaM, FroehlichJW, BlockDE, GermanJB, et al. (2010) Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem 58: 5334–5340.

60. BerryD, StecherB, SchintlmeisterA, ReichertJ, BrugirouxS, et al. (2013) Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc Natl Acad Sci U S A 110: 4720–4725.

61. McGuckinMA, LindenSK, SuttonP, FlorinTH (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9: 265–278.

62. RogosaM (1964) The Genus Veillonella. I. General Cultural, Ecological, and Biochemical Considerations. J Bacteriol 87: 162–170.

63. ChaoA (1984) Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11: 256–270.

64. ShannonCE (1948) A mathematical theory of communication. Bell System Technical Journal 27: 379–656.

65. BrayJR, CurtisJT (1957) An ordination of upland forest communities of southern Wisconsin. Ecological Monographs 27: 325–349.

66. Clements FE (1916) Plant succession: an analysis of the development of vegetation. Washington: Carnegie Institution of Washington.

67. GowerJC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53: 325–338.

68. de Berg M, van Kreveld M, Overmars M, Schwarzkopf O (2000) Computational Geometry: Algorithms and Applications. Springer-Verlag.

69. CsermelyP, KorcsmarosT, KissHJ, LondonG, NussinovR (2013) Structure and dynamics of molecular networks: a novel paradigm of drug discovery: a comprehensive review. Pharmacol Ther 138: 333–408.

70. De FilippoC, CavalieriD, Di PaolaM, RamazzottiM, PoulletJB, et al. (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107: 14691–14696.

71. ReyFE, GonzalezMD, ChengJ, WuM, AhernPP, et al. (2013) Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc Natl Acad Sci U S A 110: 13582–13587.

72. MackeyRL, CurrieDJ (2001) The Diversity-Disturbance Relationship: Is It Generally Strong and Peaked? Ecology 62: 3479–3492.

73. HobbsR, HuennekeLF (1992) Disturbance, Diversity, and Invasion: Implications for Conservation. Conservation Biology 6: 324–337.

74. Cervera-TisonM, TailfordLE, FuellC, BruelL, SulzenbacherG, et al. (2012) Functional analysis of family GH36 alpha-galactosidases from Ruminococcus gnavus E1: insights into the metabolism of a plant oligosaccharide by a human gut symbiont. Appl Environ Microbiol 78: 7720–7732.

75. DerrienM, van PasselMW, van de BovenkampJH, SchipperRG, de VosWM, et al. (2010) Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 1: 254–268.

76. NiuB, FuL, SunS, LiW (2010) Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinformatics 11: 187.

77. MavromatisK, IvanovaN, BarryK, ShapiroH, GoltsmanE, et al. (2007) Use of simulated data sets to evaluate the fidelity of metagenomic processing methods. Nat Methods 4: 495–500.

78. PignatelliM, MoyaA (2011) Evaluating the fidelity of de novo short read metagenomic assembly using simulated data. PLoS One 6: e19984.

79. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.

80. DelcherAL, BratkeKA, PowersEC, SalzbergSL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673–679.

81. FinnRD, ClementsJ, EddySR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29–37.

82. HaftDH, SelengutJD, WhiteO (2003) The TIGRFAMs database of protein families. Nucleic Acids Res 31: 371–373.

83. KarplusK, BarrettC, HugheyR (1998) Hidden Markov models for detecting remote protein homologies. Bioinformatics 14: 846–856.

84. CaporasoJG, KuczynskiJ, StombaughJ, BittingerK, BushmanFD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.

85. R Development Core Team (2010) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

86. BasualdoC (2011) Choosing the best non-parametric richness estimator for benthic macroinvertebrates databases. Rev Soc Entomol Argent 70: 27–38.

87. GrünB, KosmidisL, ZeileisA (2012) Extended Beta Regression in R: Shaken, Stirred, Mixed, and Partitioned. Journal of Statistical Software 48: 1–25.

88. ShimodairaH (2004) Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. The Annals of Statistics 32: 2343–2775.

89. KohonenT (1982) Self-Organized Formation of Topologically Correct Feature Maps. Biological Cybernetics 43: 59–69.

90. Navarro-AlbertoJ, ManlyBFJ (2009) Null model analyses of presence-absence matrices need a definition of independence. Popul Ecol 51: 505–512.

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Genetika Reprodukčná medicína

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