The Fecal Microbial Community of Breast-fed Infants from Armenia and Georgia

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Lewis, Zachery T ^a   Sidamonidze, Ketevan ^b   Tsaturyan, Vardan ^c   Tsereteli, David ^b   Khachidze, Nika ^b   Pepoyan, Astghik ^c   Zhgenti, Ekaterine ^b   Tevzadze, Liana ^b   Manvelyan, Anahit ^d   Balayan, Marine ^d   Imnadze, Paata ^b   Torok, Tamas ^e   Lemay, Danielle G ^a,e   Mills, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b National Centre for Disease Control and Public Health of Georgia   (Georgia)

^c International Association for Human and Animals Health Improvement   (Armenia)

^d ARMENIAN NATIONAL AGRARIAN UNIVERSITY   (Armenia)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARMENIA; BREAST; EXPOSURE; GEORGIA (REPUBLIC); HUMAN; INFANT; INTESTINE FLORA; LONGITUDINAL STUDY; MARKER GENE; MICROBIAL COMMUNITY; NONHUMAN; SPECIES; BIFIDOBACTERIUM; BREAST FEEDING; FECES; FEMALE; GENETICS; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY; NEWBORN;

RNA 16S;

ARMENIA; BIFIDOBACTERIUM; BREAST FEEDING; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; GEORGIA (REPUBLIC); HUMANS; INFANT; INFANT, NEWBORN; MALE; RNA, RIBOSOMAL, 16S;

EID: 85011383103     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep40932     Document Type: Article

References (78)

1. Rook, G. a W., Raison, C. L. & Lowry, C. a. Microbial Old Friends, immunoregulation and socio-economic status. Clin. Exp. Immunol. 1-24, doi: 10.1111/cei.12269 (2014).
2. Hanson, L. A. et al. Protective factors in milk and the development of the immune system. Pediatrics 75, 172-176 (1985).
3. Brown, E. M., Arrieta, M.-C. & Finlay, B. B. A fresh look at the hygiene hypothesis: how intestinal microbial exposure drives immune effector responses in atopic disease. Semin. Immunol. 25, 378-87 (2013).
4. Bäckhed, F. et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 12, 611-22 (2012).
5. Scholtens, P. A. M. J., Oozeer, R., Martin, R., Amor, K. Ben & Knol, J. The Early Settlers: Intestinal Microbiology in Early Life. Annu. Rev. Food Sci. Technol. 3, 425-447 (2012).
6. Hickey, R. M. The role of oligosaccharides from human milk and other sources in prevention of pathogen adhesion. Int. Dairy J. 22, 141-146 (2012).
7. Zivkovic, A. M., Lewis, Z. T., German, J. B. & Mills, D. A. Establishment of a Milk-Oriented Microbiota ( MOM ) in early life : How Babies Meet Their MOMs. Funct. Food Rev. 5, 3-12 (2013).
8. Kunz, C. & Rudloff, S. Health promoting aspects of milk oligosaccharides. Int. Dairy J. 16, 1341-1346 (2006).
9. Garrido, D., Dallas, D. C. & Mills, D. a. Consumption of human milk glycoconjugates by infant-Associated bifidobacteria: mechanisms and implications. Microbiology 159, 649-64 (2013).
10. Sela, D. A. & Mills, D. A. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 18, 298-307 (2010).
11. Zivkovic, A. M., German, J. B., Lebrilla, C. B. & Mills, D. a. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc. Natl. Acad. Sci. USA 108 Suppl, 4653-8 (2011).
12. Sela, D. A. et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. USA 105, 18964-9 (2008).
13. Garrido, D., Kim, J. H., German, J. B., Raybould, H. E. & Mills, D. A. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One 6, e17315 (2011).
14. Sela, D. A. et al. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl. Environ. Microbiol. 78, 795-803 (2012).
15. Asakuma, S. et al. Physiology of consumption of human milk oligosaccharides by infant gut-Associated bifidobacteria. J. Biol. Chem. 286, 34583-92 (2011).
16. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222-227 (2012).
17. Fukuda, S. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543-7 (2011).
18. Sheil, B. et al. Role of interleukin (IL-10) in probiotic-mediated immune modulation: An assessment in wild-Type and IL-10 knockout mice. Clin. Exp. Immunol. 144, 273-80 (2006).
19. Tanabe, S., Kinuta, Y. & Saito, Y. Bifidobacterium infantis suppresses proinflammatory interleukin-17 production in murine splenocytes and dextran sodium sulfate-induced intestinal inflammation. Int. J. Mol. Med. 22, 181-185 (2008).
20. Preising, J. et al. Selection of bifidobacteria based on adhesion and anti-inflammatory capacity in vitro for amelioration of murine colitis. Appl. Environ. Microbiol. 76, 3048-51 (2010).
21. Chichlowski, M., De Lartigue, G., German, J. B., Raybould, H. E. & Mills, D. a. Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J. Pediatr. Gastroenterol. Nutr. 55, 321-7 (2012).
22. Huda, M. N. et al. Stool Microbiota and Vaccine Responses of Infants. Pediatrics 134, e362-72 (2014).
23. Matsuki, T. et al. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat. Commun. 7, 11939 (2016).
24. Lewis, Z. T. et al. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome 3 (2015).
25. Chichlowski, M., German, J. B., Lebrilla, C. B. & Mills, D. A. The influence of milk oligosaccharides on microbiota of infants: opportunities for formulas. Annu. Rev. Food Sci. Technol. 2, 331-51 (2011).
26. Avershina, E. et al. Major fecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiol. Ecol. 87, 280-90 (2014).
27. Abrahamsson, T. R. et al. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin. Exp. Allergy 44, 842-50 (2014).
28. Azad, M. B. et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ 185, 385-394 (2013).
29. Roos, S. et al. 454 pyrosequencing analysis on faecal samples from a randomized DBPC trial of colicky infants treated with Lactobacillus reuteri DSM 17938. PLoS One 8, e56710 (2013).
30. Jost, T., Lacroix, C., Braegger, C. P. & Chassard, C. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS One 7, e44595 (2012).
31. Lewis, Z. T. et al. Maternal Fucosyltransferase 2 Status Affects the Gut Bifidobacterial Communities of Breastfed Infants. Microbiome 3, 1-21 (2015).
32. Grześkowiak, L. et al. Distinct gut microbiota in southeastern African and northern European infants. J. Pediatr. Gastroenterol. Nutr. 54, 812-6 (2012).
33. Lewis, Z. T. et al. The impact of freeze-drying infant fecal samples on measures of their bacterial community profiles and milkderived oligosaccharide content. PeerJ 4, e1612 (2016).
34. Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS 108, 4516-4522 (2011).
35. Caporaso, J. G. et al. QIIME allows analysis of high-Throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
36. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-1 (2010).
37. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-7 (2007).
38. Cole, J. R. et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141-5 (2009).
39. DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-72 (2006).
40. Caporaso, J. G. et al. PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-7 (2010).
41. Price, M. N., Dehal, P. S. & Arkin, A. P. Fasttree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650 (2009).
42. Lozupone, C. A., Hamady, M., Kelley, S. T. & Knight, R. Quantitative and qualitative B diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 73, 1576-1585 (2007).
43. Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32-46 (2001).
44. Paulson, J. N., Stine, O. C., Bravo, H. C. & Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10, 1200-2 (2013).
45. Liu, Z., Desantis, T. Z., Andersen, G. L. & Knight, R. Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequencers. Nucleic Acids Res. 36, 1-11 (2008).
46. Lewis, Z. T. et al. Use of bifidobacterial specific terminal restriction fragment length polymorphisms to complement next generation sequence profiling of infant gut communities. Anaerobe 19, 62-9 (2013).
47. Lewis, Z. T. et al. Validating bifidobacterial species and subspecies identity in commercial probiotic products. Pediatr. Res. 1-8, doi: 10.1038/pr.2015.244 (2015).
48. Biasucci, G., Benenati, B., Morelli, L., Bessi, E. & Boehm, G. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr 138, 1796S-1800S (2008).
49. Bäckhed, F. et al. Defining a Healthy Human Gut Microbiome: Current Concepts, Future Directions, and Clinical Applications. Cell Host Microbe 12, 611-622 (2012).
50. Subramanian, S. et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510, 417-421 (2014).
51. Marques, T. M. et al. Programming infant gut microbiota: influence of dietary and environmental factors. Curr. Opin. Biotechnol. 21, 149-56 (2010).
52. Koenig, J. E. et al. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA 108, 4578-85 (2011).
53. Lawley, T. D. & Walker, A. W. Intestinal colonization resistance. Immunology 138, 1-11 (2012).
54. Elahi, S. et al. Immunosuppressive CD71+ erythroid cells compromise neonatal host defence against infection. Nature 504, 158-162 (2013).
55. Trivers, R. L. Parent-Offspring Conflict. Am. Zool. 14, 249-264 (1974).
56. CIA World Factbook. At https://www.cia.gov/library/publications/the-world-factbook/geos/gg.html.
57. Fouhy, F. et al. High-Throughput sequencing reveals the incomplete, short-Term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob. Agents Chemother. 56, 5811-20 (2012).
58. Community-Associated methicillin-resistant Staphylococcus aureus infection among healthy newborns-Chicago and Los Angeles County, 2004. MMWR Morb Mortal Wkly Rep 55, 329-332 (2006).
59. Huurre, A. et al. Mode of Delivery-Effects on Gut Microbiota and Humoral Immunity. Neonatology 93, 236-240 (2008).
60. Hickey, R. J., Zhou, X., Pierson, J. D., Ravel, J. & Forney, L. J. Understanding vaginal microbiome complexity from an ecological perspective. Transl. Res. 160, 267-82 (2012).
61. Bode, L. Human Milk Oligosaccharides: Every Baby needs a Sugar Mama. Glycobiology 22, 1147-62 (2012).
62. Yu, Z.-T. et al. The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 23, 169-77 (2013).
63. De Leoz, M. L. A. et al. Human Milk Glycomics and Gut Microbial Genomics in Infant Feces Shows Correlation between Human Milk Oligosaccharides and Gut Microbiota: A Proof-of-Concept Study. J. Proteome Res., doi: 10.1021/pr500759e (2014).
64. Wang, M. et al. Fecal microbiota composition of breast-fed infants is correlated with human milk oligosaccharides consumed. J. Pediatr. Gastroenterol. Nutr. 60, 825-33 (2015).
65. Ruiz-Moyano, S. et al. Variation in Consumption of Human Milk Oligosaccharides by Infant Gut-Associated Strains of Bifidobacterium breve. Appl. Environ. Microbiol. 79, 6040-9 (2013).
66. Avershina, E. et al. Bifidobacterial succession and correlation networks in a large unselected cohort of mothers and their children. Appl. Environ. Microbiol. 79, 497-507 (2013).
67. Bottacini, F. et al. Comparative genomics of the Bifidobacterium breve taxon. BMC Genomics 15, 170 (2014).
68. LoCascio, R. G., Desai, P., Sela, D. A., Weimer, B. & Mills, D. A. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Appl. Environ. Microbiol. 76, 7373-81 (2010).
69. Maynard, C. L., Elson, C. O., Hatton, R. D. & Weaver, C. T. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489, 231-41 (2012).
70. Grönlund, M.-M. et al. Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the Bifidobacterium microbiota in infants at risk of allergic disease. Clin. Exp. Allergy 37, 1764-72 (2007).
71. Wacklin, P. et al. Faecal Microbiota Composition in Adults Is Associated with the FUT2 Gene Determining the Secretor Status. PLoS One 9, e94863 (2014).
72. Tong, M. et al. Reprograming of gut microbiome energy metabolism by the FUT2 Crohns disease risk polymorphism. ISME J. 1-14, doi: 10.1038/ismej.2014.64 (2014).
73. Rausch, P. et al. Colonic mucosa-Associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc. Natl. Acad. Sci. USA 108, 19030-19035 (2011).
74. Wacklin, P. et al. Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PLoS One 6, e20113 (2011).
75. Newburg, D. S., Ruiz-Palacios, G. M. & Morrow, A. L. Human milk glycans protect infants against enteric pathogens. Annu. Rev. Nutr. 25, 37-58 (2005).
76. Newburg, D. S. et al. Innate protection conferred by fucosylated oligosaccharides of human milk against diarrhea in breastfed infants. Glycobiology 14, 253-63 (2004).
77. Egan, M. et al. Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium. BMC Microbiol. 14, 282 (2014).
78. Egan, M., OConnell Motherway, M., Ventura, M. & van Sinderen, D. Metabolism of sialic acid by Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 80, 4414-4426 (2014).