Gut microbial gene expression in mother-fed and formula-fed piglets

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Poroyko, Valeriy ^a   White, James Robert ^b   Wang, Mei ^c   Donovan, Sharon ^c   Alverdy, John ^a   Liu, Donald C ^a   Morowitz, Michael J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b Bldg 142   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; DNA 16S; RNA 16S; BACTERIAL DNA; COMPLEMENTARY DNA;

AMINO ACID METABOLISM; AMPLICON; ANIMAL TISSUE; ARTICLE; ARTIFICIAL MILK; BACTEROIDES; BREAST MILK; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DNA SEQUENCE; GENE EXPRESSION; INFANT NUTRITION; INTESTINE FLORA; MICROBIAL COMMUNITY; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PIGLET; PREVOTELLA; PROTEIN METABOLISM; RNA SEQUENCE; ANIMAL; ANIMAL FOOD; BACTERIUM; CECUM; CLASSIFICATION; GENE EXPRESSION PROFILING; GENETICS; MICROBIOLOGY; MOTHER; SWINE;

ANIMALIA; BACTEROIDES; PREVOTELLA;

ANIMAL FEED; ANIMALS; ANIMALS, NEWBORN; BACTERIA; CECUM; DNA, BACTERIAL; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; INFANT FORMULA; MOTHERS; SEQUENCE ANALYSIS, DNA; SWINE;

EID: 77957927457     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012459     Document Type: Article

References (74)

1. Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69: 1035S-45S.
2. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, et al. (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118: 511-21.
3. Palmer C, Bik EM, Digiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5: e177.
4. Lundequist B, Nord CE, Winberg J (1985) The composition of the faecal microflora in breastfed and bottle fed infants from birth to eight weeks. Acta Paediatr Scand 1985 74: 45-51.
5. Hopkins MJ, Macfarlane GT, Furrie E, Fite A, Macfarlane S (2005) Characterisation of intestinal bacteria in infant stools using real-time PCR and northern hybridisation analyses. FEMS Microbiol Ecol 54: 77-85.
6. Penders J, Vink C, Driessen C, London N, Thijs C, et al. (2005) Quantification of bifidobacterium spp., escherichia coli and clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett 243: 141-7.
7. Morales Y, Schanler RJ (2007) Human milk and clinical outcomes in VLBW infants: How compelling is the evidence of benefit? Semin Perinatol 31: 83-8.
8. Lin PW, Stoll BJ (2006) Necrotising enterocolitis. Lancet 368: 1271-83.
9. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
10. Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, et al. (2008) Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One 3: e2836.
11. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, et al. (2008) Functional metagenomic profiling of nine biomes. Nature 452: 629-32.
12. 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: 1388-92.
13. Verberkmoes NC, Russell AL, Shah M, Godzik A, Rosenquist M, et al. (2009) Shotgun metaproteomics of the human distal gut microbiota. ISME J 3: 179-89.
14. Jansson J, Willing B, Lucio M, Fekete A, Dicksved J, et al. (2009) Metabolomics reveals metabolic biomarkers of crohn's disease. PLoS One 4: e6386.
15. Saric J, Wang Y, Li J, Coen M, Utzinger J, et al. (2008) Species variation in the fecal metabolome gives insight into differential gastrointestinal function. J Proteome Res 7: 352-60.
16. Turnbaugh P, Ridaura VK, Faith JJ, Rey FE, Knight R, et al. (2009) The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Science Translational Medicine 1: 6.
17. Turnbaugh PJ, Quince C, Faith JJ, McHardy AC, Yatsunenko T, et al. (2010) Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci USA 107: 7503-8.
18. Gilbert JA, Field D, Huang Y, Edwards R, Li W, et al. (2008) Detection of large numbers of novel sequences in the metatranscriptomes of complex marine microbial communities. PLoS ONE 3: e3042.
19. Shi Y, Tyson GW, DeLong EF (2009) Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459: 266-9.
20. Poretsky RS, Hewson I, Sun S, Allen AE, Zehr JP, et al. (2009) Comparative day/night metatranscriptomic analysis of microbial communities in the north pacific subtropical gyre. Environ Microbiol 11: 1358-75.
21. Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, et al. (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci 105: 3805-10.
22. Leininger S, Urich T, Schloter M, Schwark L, Qi J, et al. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-9.
23. Urich T, Lanzen A, Qi J, Huson DH, Schleper C, et al. (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3: e2527.
24. Wang Z, Gerstein M, Snyder M (2009) RNA-seq: A revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
25. van Vliet AH (2009) Next generation sequencing of microbial transcriptomes: Challenges and opportunities. FEMS Microbiol Lett 302: 1-7.
26. Yoder-Himes DR, Chain PS, Zhu Y, Wurtzel O, Rubin EM, et al. (2009) Mapping the burkholderia cenocepacia niche response via high-throughput sequencing. Proc Natl Acad Sci 106: 3976-81.
27. Shelburne SA, 3rd, Keith D, Horstmann N, Sumby P, Davenport MT, et al. (2008) A direct link between carbohydrate utilization and virulence in the major human pathogen group A streptococcus. Proc Natl Acad Sci 105: 1698-703.
28. Gorke B, Stulke J (2008) Carbon catabolite repression in bacteria: Many ways to make the most out of nutrients. Nat Rev Micro 6: 613-24.
29. White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5: e1000352.
30. 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: 5261-7.
31. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, et al. (2009) A core gut microbiome in obese and lean twins. Nature 457: 480-4.
32. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, et al. (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14: 169-81.
33. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, et al. (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386.
34. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278: 631-7.
35. Letunic I, Yamada T, Kanehisa M, Bork P (2008) iPath: Interactive exploration of biochemical pathways and networks. Trends Biochem Sci 33: 101-3.
36. Kurtz DM Jr. (2006) Avoiding high-valent iron intermediates: Superoxide reductase and rubrerythrin. J Inorg Biochem 100: 679-93.
37. Martens EC, Koropatkin NM, Smith TJ, Gordon JI (2009) Complex glycan catabolism by the human gut microbiota: The bacteroidetes sus-like paradigm. J Biol Chem 284: 24673-7.
38. Terra VS, Homer KA, Rao SG, Andrew PW, Yesilkaya H (2010) Characterization of novel {beta}-galactosidase activity that contributes to glycoprotein degradation and virulence in streptococcus pneumoniae. Infect Immun 78: 348-57.
39. Ge J, Catt DM, Gregory RL (2004) Streptococcus mutans surface alpha-enolase binds salivary mucin MG2 and human plasminogen. Infect Immun 72: 6748-52.
40. Candela M, Biagi E, Centanni M, Turroni S, Vici M, et al. (2009) Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiology 155: 3294-303.
41. Candela M, Bergmann S, Vici M, Vitali B, Turroni S, et al. (2007) Binding of human plasminogen to bifidobacterium. J Bacteriol 189: 5929-36.
42. Granato D, Bergonzelli GE, Pridmore RD, Marvin L, Rouvet M, et al. (2004) Cell surface-associated elongation factor tu mediates the attachment of lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 72: 2160-9.
43. Sanchez B, Schmitter JM, Urdaci MC (2009) Identification of novel proteins secreted by Lactobacillus plantarum that bind to mucin and fibronectin. J Mol Micro Biotech 17: 158-162.
44. Egea L, Aguilera L, Gimenez R, Sorolla MA, Aguilar J, et al. (2007) Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic escherichia coli: Interaction of the extracellular enzyme with human plasminogen and fibrinogen. Int J Biochem Cell Biol 39: 1190-203.
45. Lerner A, Castro-Sowinski S, Valverde A, Lerner H, Dror R, et al. (2009) The azospirillum brasilense Sp7 noeJ and noeL genes are involved in extracellular polysaccharide biosynthesis. Microbiology 155: 4058-68.
46. Mailloux RJ, Singh R, Brewer G, Auger C, Lemire J, et al. (2009) Alphaketoglutarate dehydrogenase and glutamate dehydrogenase work in tandem to modulate the antioxidant alpha-ketoglutarate during oxidative stress in pseudomonas fluorescens. J Bacteriol 191: 3804-10.
47. Goldberg JB, Hatano K, Pier GB (1993) Synthesis of lipopolysaccharide O side chains by pseudomonas aeruginosa PAO1 requires the enzyme phosphomannomutase. J Bacteriol 175: 1605-11.
48. Houot L, Chang S, Absalon C, Watnick PI (2010) Vibrio cholerae phosphoenolpyruvate phosphotransferase system control of carbohydrate transport, biofilm formation, and colonization of the germfree mouse intestine. Infect Immun 78: 1482-94.
49. Fugier E, Salcedo SP, de Chastellier C, Pophillat M, Muller A, et al. (2009) The glyceraldehyde-3-phosphate dehydrogenase and the small GTPase rab 2 are crucial for brucella replication. PLoS Pathog 5: e1000487.
50. Schutte JB, de Jong J, van Weerden EJ, Tamminga S (1992) Nutritional implications of L-arabinose in pigs. Br J Nutr 68: 195-207.
51. Vaillancourt K, Bedard N, Bart C, Tessier M, Robitaille G, et al. (2008) Role of galK and galM in galactose metabolism by streptococcus thermophilus. Appl Environ Microbiol 74: 1264-7.
52. Sasajima K, Kumada T (1983) Deficiency of flagellation in a bacillus subtilis pleiotropic mutant lacking transketolase. Agric Biol Chem 47: 1375-6.
53. Eidels L, Osborn MJ (1971) Lipopolysaccharide and aldoheptose biosynthesis in transketolase mutants of salmonella typhimurium. Proc Natl Acad Sci 68: 1673-7.
54. Gonzalez 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: 4686-94.
55. Bertolo RF, Burrin DG (2008) Comparative aspects of tissue glutamine and proline metabolism. J Nutr 138: 2032S-9S.
56. Aycicek A, Erel O, Kocyigit A, Selek S, Demirkol MR (2006) Breast milk provides better antioxidant power than does formula. Nutrition 22: 616-9.
57. Friel JK, Martin SM, Langdon M, Herzberg A, Gene R, et al. (2002) Milk from mothers of both premature and full-term infants provides better antioxidant protection than does infant formula. Pediatr Res 51: 612-8.
58. Tsolis RM, Baumler AJ, Heffron F, Stojilkovic I (1996) Contribution of TonBand Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect Immun 64: 4549-56.
59. Torres AG, Redford P, Welch RA, Payne SM (2001) Ton-B dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun 69: 6179-85.
60. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292: 1115-8.
61. Sears CL (2005) A dynamic partnership: Celebrating our gut flora. Anaerobe 11: 247-51.
62. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, et al. (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291: 881-4.
63. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, et al. (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15: 1016-22.
64. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci 102: 11070-5.
65. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104: 13780-5.
66. Frank DN, Pace NR (2008) Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 24: 4-10.
67. Allen EE, Banfield JF (2005) Community genomics in microbial ecology and evolution. Nat Rev Microbiol 3: 489-98.
68. Prangli AL, Utt M, Talja I, Sepp E, Mikelsaar M, et al. (2009) Antigenic proteins of lactobacillus acidophilus that are recognised by serum IgG antibodies in children with type 1 diabetes and coeliac disease. Pediatr Allergy Immunol. Epub ahead of print Jul 2.
69. Shah P, Shah V (2007) Arginine supplementation for prevention of necrotising enterocolitis in preterm infants. Cochrane Database Syst Rev 3: CD004339.
70. Amin HJ, Zamora SA, McMillan DD, Fick GH, Butzner JD, et al. (2002) Arginine supplementation prevents necrotizing enterocolitis in the premature infant. J Pediatr 140: 425-31.
71. Houle VM, Schroeder EA, Odle J, Donovan SM (1997) Small intestinal disaccharidase activity and ileal villus height are increased in piglets consuming formula containing recombinant human insulin-like growth factor-I. Pediatr Res 42: 78-86.
72. Zoetendal EG, Heilig HG, Klaassens ES, Booijink CC, Kleerebezem M, et al. (2006) Isolation of DNA from bacterial samples of the human gastrointestinal tract. Nat Protoc 1: 870-3.
73. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al. (2007) SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucl Acids Res 35: 7188-96.
74. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The ribosomal database project: Improved alignments and new tools for rRNA analysis. Nucl Acids Res 37: D141-145.