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References

  1. Allen J, Hector D. 2005. Benefits of breastfeeding. NSW Public Health Bull. 16: 42-46.
    CrossRef
  2. B äckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
  3. Berseth CL, Thureen PJ, Hay WW. 2006. Development of the gastrointestinal tract. Neonatal Nutr. Metab. 2: 67-73.
    CrossRef
  4. B ezirtzoglou E, Tsiotsias A, Welling GW. 2011. Microbiota profile in feces of breast-and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 17:478-482.
    CrossRef
  5. B iasucci G, Benenati B, Morelli L, Bessi E, Boehm G. 2008. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J. Nutr. 138: 1796S-1800S.
  6. B iasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. 2010. Mode of delivery affects the bacterial community in the newborn gut. Early Hum. Dev. 86: S13S15.
  7. Chao A, Shen TJ. 2003. Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ. Ecol. Stat. 10: 429-443.
    CrossRef
  8. Cl aesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, et al. 2011. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl. Acad. Sci. USA 108: 4586-4591.
  9. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. 2011. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 107:14691-14696.
    CrossRef
  10. de la Cochetiere MF, Piloquet H, des Robert C, Darmaun D, Galmiche JP, Roze JC. 2004. Early intestinal bacterial colonization and necrotizing enterocolitis in infants: the putative role of Clostridium. Pediatr. Res. 56: 366-370.
    CrossRef
  11. Delzenne NM, Neyrinck AM, Bäckhed F, Cani PD. 2011. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat. Rev. Endocrinol. 7: 639-646.
    CrossRef
  12. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. 2005. Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
    CrossRef
  13. Fabrice A, Didier R. 2009. Exploring microbial diversity using 16S rRNA high-throughput methods. J. Comput. Sci. Syst. Biol. 2: 074-092.
  14. Fallani M, Young D, Scott J , Norin E, Amarri S, Adam R, et al. 2010. Intestinal microbiota of 6-week-old infants across Europe:geographic influence beyond delivery mode, breastfeeding, and antibiotics. J. Pediatr. Gastroenterol. Nutr. 51: 77-84.
    CrossRef
  15. Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM. 2013. The human milk microbiota:origin a nd p otential r oles in h ealth and disease. Pharmacol. Res. 69: 1-10.
    CrossRef
  16. Fox PF, Kelly AL. 2006. Indigenous enzymes in milk:overview and historical aspects-Part - 2 . Int. Dairy J. 16:517-532.
    CrossRef
  17. González R, Klaassens ES, Malinen E, de Vos WM, Vaughan EE. 2008. Differential transcriptional response of Bifidobacterium longum to human milk, formula milk, and galactooligosaccharide. Appl. Environ. Microbiol. 74: 4686-4694.
    CrossRef
  18. Haraszthy VI, Zambon JJ, Sreenivasan PK, Zambon MM, Gerber D, Rego R, Parker C. 2007. Identification of oral bacterial species associated with halitosis. J. Am. Dent. Assoc. 138: 1113-1120.
  19. Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, et al. 2007. The fecal microbiota of irritable bowel sydrome patients differs significantly from that of healthy subjects. Gastroenterology 133: 24-33.
    CrossRef
  20. Klaassens ES, de Vos WM, Vaughan EE. 2007. Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract. Appl. Environ. Microbiol. 73: 1388-1392.
    CrossRef
  21. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, et al. 2011. Microbes and health sackler colloquium:succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA 108: 4578-4585.
    CrossRef
  22. Lecuit M, Suarez F, Lortholary O. 2004. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. Med. Sci. 20: 638-640.
  23. Martín R, Langa S, Reviriego C, Jiminez E, Marín ML, Xaus J, et al. 2003. Human milk i s a source of lactic acid bacteria for the infant gut. J. Pediatr. 143: 754-758.
    CrossRef
  24. Martín R, Heilig GHJ, Zoetendal EG, Smidt H, Rodriguez JM. 2007. Diversity of the Lactobacillus group in breast milk and vagina of healthy women and potential role in the colonization of the infant gut. J. Appl. Microbiol. 103: 26382644.
    CrossRef
  25. Moore TA, Hanson CK, Anderson-Berry A. 2011. Colonization of the gastrointestinal tract in neonates: a review. ICAN 3:291-295.
  26. Morelli L. 2008. Postnatal development of intestinal microflora as influenced by infant nutrition. J. Nutr. 138: 1791S-1795S.
  27. Neu J, Rushing J. 2011. Cesarean versus vaginal delivery:long-term infant outcomes and the hygiene hypothesis. Clin. Perinatol. 38: 321-331.
    CrossRef
  28. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PLoS Biol. 5: e177.
    CrossRef
  29. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK. 1991. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl. J. Med. 325: 1127-1131.
    CrossRef
  30. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. 2005. Quantification of Bifidobacterium spp. , Escherichia and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol. Lett. 243: 141-147.
    CrossRef
  31. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. 2010. A h uman g ut microbial g ene catalogue established by metagenomic sequencing. Nature 464: 59-65.
    CrossRef
  32. Reetta MS, Elaine EV, Christine FF, Joël Doré CE, de VOS VM. 2002. Diversity of Bidobacterium and Lactobacillus spp. In breast-fed and formula-fed infants as assessed by 16S rDNA sequence differences. Microb. Ecol. Health Dis. 14: 97105.
  33. Rinne M, Kalliomaki M, Arvilommi H, Salminen S, Isolauri E. 2005. Effect of probiotics and breastfeeding on the Bifidobacterium and Lactobacillus/Enterococcus microbiota and humoral immune responses. J. Pediatr. 147: 186-191.
    CrossRef
  34. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541.
    CrossRef
  35. Sinkiewicz G, Ljunggren L. 2008. Occurrence of Lactobacillus reuteri in human breast milk. Microb. Ecol. Health Dis. 20:122-126.
    CrossRef
  36. Sokol H, Pigneur B, Watterlot L, Lakhdari O, BermúdezHumarán LG, Gratadoux JJ, et al. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA 105: 16731-16736.
    CrossRef
  37. Tamboli CP, Neut C, Desreumaux P, Colombel JF. 2004. Dysbiosis in inflammatory bowel disease. Gut 53: 1-4.
    CrossRef
  38. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 10271031.
    CrossRef
  39. Turroni F, Foroni E, Pizzetti P, Giubellini V, Ribbera A, Merusi P, et al. 2009. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl. Environ. Microbiol. 75: 1534-1545.
    CrossRef
  40. Waar K, Degener JE, van Luyn MJ, Harmsen HJ. 2005. Fluorescence in situ hybridization with specific DNA probes offers adequate detection of Enterococcus faecalis and Enterococcus faecium in clinical samples. J. Med. Microbiol. 54:937-944.
    CrossRef
  41. 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: 5261-5267.
    CrossRef
  42. Young VB. 2012. The intestinal microbiota in health and disease. Curr. Opin. Gastroenterol. 28: 63-69.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(2): 133-143

Published online February 28, 2014 https://doi.org/10.4014/jmb.1309.09029

Copyright © The Korean Society for Microbiology and Biotechnology.

Impact of Diet in Shaping Gut Microbiota Revealed by a Comparative Study in Infants During the Six Months of Life

Wenguang Fan 1, 2, Guicheng Huo 1*, Xiaomin Li 1, Lijie Yang 1 and Cuicui Duan 1

1Key Laboratory of Dairy Science, Ministry of Education, Northeast Agricultural University,Harbin 150030,China, 2 Hei LongJiang Vocational College, Harbin 150111, China

Received: September 12, 2013; Accepted: October 28, 2013

Abstract

The development of the gut is controlled and modulated by different interacting mechanisms,
such as genetic endowment, intrinsic biological regulatory functions, environment influences
and last but no least, the diet influence. In this work, we compared the fecal microbiota of
breast-fed (BF), formula-fed (FF), and mixed-fed (MF) infants from Hebei Province, China. By
using high-throughput 16S rDNA sequencing analyses, we found some differences in gut
microbiota in the three groups. Firmicutes and Proteobacteria were the dominant bacteria at
the phylum level in the three groups, where FF infants showed a significant depletion in
Bacteroidetes (p < 0.001) and Actinobacteria (p < 0.05). Enterobacteriaceae was the dominant
bacteria at the family level in the three groups, but FF infants showed higher Enterobacteriaceae
enrichment than BF and MF infants (p < 0.05); the abundance of the Bifidobacteriaceae was
only 8.16% in the feces of BF infants, but higher than in MF and FF infants (p < 0.05). The
number of genera detected (abundance >0.01%) in BF, MF, and FF infants was only 15, 16, and
13, respectively. This study could provide more accurate and scientific data for the future
study of infant intestinal flora.

Keywords: infant intestinal microbiota, breast-fed, formula-fed, mixed-fed, high-throughput sequencing

References

  1. Allen J, Hector D. 2005. Benefits of breastfeeding. NSW Public Health Bull. 16: 42-46.
    CrossRef
  2. B äckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
  3. Berseth CL, Thureen PJ, Hay WW. 2006. Development of the gastrointestinal tract. Neonatal Nutr. Metab. 2: 67-73.
    CrossRef
  4. B ezirtzoglou E, Tsiotsias A, Welling GW. 2011. Microbiota profile in feces of breast-and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 17:478-482.
    CrossRef
  5. B iasucci G, Benenati B, Morelli L, Bessi E, Boehm G. 2008. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J. Nutr. 138: 1796S-1800S.
  6. B iasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. 2010. Mode of delivery affects the bacterial community in the newborn gut. Early Hum. Dev. 86: S13S15.
  7. Chao A, Shen TJ. 2003. Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ. Ecol. Stat. 10: 429-443.
    CrossRef
  8. Cl aesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, et al. 2011. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl. Acad. Sci. USA 108: 4586-4591.
  9. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. 2011. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 107:14691-14696.
    CrossRef
  10. de la Cochetiere MF, Piloquet H, des Robert C, Darmaun D, Galmiche JP, Roze JC. 2004. Early intestinal bacterial colonization and necrotizing enterocolitis in infants: the putative role of Clostridium. Pediatr. Res. 56: 366-370.
    CrossRef
  11. Delzenne NM, Neyrinck AM, Bäckhed F, Cani PD. 2011. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat. Rev. Endocrinol. 7: 639-646.
    CrossRef
  12. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. 2005. Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
    CrossRef
  13. Fabrice A, Didier R. 2009. Exploring microbial diversity using 16S rRNA high-throughput methods. J. Comput. Sci. Syst. Biol. 2: 074-092.
  14. Fallani M, Young D, Scott J , Norin E, Amarri S, Adam R, et al. 2010. Intestinal microbiota of 6-week-old infants across Europe:geographic influence beyond delivery mode, breastfeeding, and antibiotics. J. Pediatr. Gastroenterol. Nutr. 51: 77-84.
    CrossRef
  15. Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM. 2013. The human milk microbiota:origin a nd p otential r oles in h ealth and disease. Pharmacol. Res. 69: 1-10.
    CrossRef
  16. Fox PF, Kelly AL. 2006. Indigenous enzymes in milk:overview and historical aspects-Part - 2 . Int. Dairy J. 16:517-532.
    CrossRef
  17. González R, Klaassens ES, Malinen E, de Vos WM, Vaughan EE. 2008. Differential transcriptional response of Bifidobacterium longum to human milk, formula milk, and galactooligosaccharide. Appl. Environ. Microbiol. 74: 4686-4694.
    CrossRef
  18. Haraszthy VI, Zambon JJ, Sreenivasan PK, Zambon MM, Gerber D, Rego R, Parker C. 2007. Identification of oral bacterial species associated with halitosis. J. Am. Dent. Assoc. 138: 1113-1120.
  19. Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, et al. 2007. The fecal microbiota of irritable bowel sydrome patients differs significantly from that of healthy subjects. Gastroenterology 133: 24-33.
    CrossRef
  20. Klaassens ES, de Vos WM, Vaughan EE. 2007. Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract. Appl. Environ. Microbiol. 73: 1388-1392.
    CrossRef
  21. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, et al. 2011. Microbes and health sackler colloquium:succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA 108: 4578-4585.
    CrossRef
  22. Lecuit M, Suarez F, Lortholary O. 2004. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. Med. Sci. 20: 638-640.
  23. Martín R, Langa S, Reviriego C, Jiminez E, Marín ML, Xaus J, et al. 2003. Human milk i s a source of lactic acid bacteria for the infant gut. J. Pediatr. 143: 754-758.
    CrossRef
  24. Martín R, Heilig GHJ, Zoetendal EG, Smidt H, Rodriguez JM. 2007. Diversity of the Lactobacillus group in breast milk and vagina of healthy women and potential role in the colonization of the infant gut. J. Appl. Microbiol. 103: 26382644.
    CrossRef
  25. Moore TA, Hanson CK, Anderson-Berry A. 2011. Colonization of the gastrointestinal tract in neonates: a review. ICAN 3:291-295.
  26. Morelli L. 2008. Postnatal development of intestinal microflora as influenced by infant nutrition. J. Nutr. 138: 1791S-1795S.
  27. Neu J, Rushing J. 2011. Cesarean versus vaginal delivery:long-term infant outcomes and the hygiene hypothesis. Clin. Perinatol. 38: 321-331.
    CrossRef
  28. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. 2007. Development of the human infant intestinal microbiota. PLoS Biol. 5: e177.
    CrossRef
  29. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK. 1991. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl. J. Med. 325: 1127-1131.
    CrossRef
  30. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. 2005. Quantification of Bifidobacterium spp. , Escherichia and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol. Lett. 243: 141-147.
    CrossRef
  31. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. 2010. A h uman g ut microbial g ene catalogue established by metagenomic sequencing. Nature 464: 59-65.
    CrossRef
  32. Reetta MS, Elaine EV, Christine FF, Joël Doré CE, de VOS VM. 2002. Diversity of Bidobacterium and Lactobacillus spp. In breast-fed and formula-fed infants as assessed by 16S rDNA sequence differences. Microb. Ecol. Health Dis. 14: 97105.
  33. Rinne M, Kalliomaki M, Arvilommi H, Salminen S, Isolauri E. 2005. Effect of probiotics and breastfeeding on the Bifidobacterium and Lactobacillus/Enterococcus microbiota and humoral immune responses. J. Pediatr. 147: 186-191.
    CrossRef
  34. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541.
    CrossRef
  35. Sinkiewicz G, Ljunggren L. 2008. Occurrence of Lactobacillus reuteri in human breast milk. Microb. Ecol. Health Dis. 20:122-126.
    CrossRef
  36. Sokol H, Pigneur B, Watterlot L, Lakhdari O, BermúdezHumarán LG, Gratadoux JJ, et al. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA 105: 16731-16736.
    CrossRef
  37. Tamboli CP, Neut C, Desreumaux P, Colombel JF. 2004. Dysbiosis in inflammatory bowel disease. Gut 53: 1-4.
    CrossRef
  38. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 10271031.
    CrossRef
  39. Turroni F, Foroni E, Pizzetti P, Giubellini V, Ribbera A, Merusi P, et al. 2009. Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl. Environ. Microbiol. 75: 1534-1545.
    CrossRef
  40. Waar K, Degener JE, van Luyn MJ, Harmsen HJ. 2005. Fluorescence in situ hybridization with specific DNA probes offers adequate detection of Enterococcus faecalis and Enterococcus faecium in clinical samples. J. Med. Microbiol. 54:937-944.
    CrossRef
  41. 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: 5261-5267.
    CrossRef
  42. Young VB. 2012. The intestinal microbiota in health and disease. Curr. Opin. Gastroenterol. 28: 63-69.
    CrossRef