Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Saulnier, Delphine M ^a,d   Santos, Filipe ^b,c   Roos, Stefan ^e   Mistretta, Toni Ann ^a   Spinler, Jennifer K ^a,d   Molenaar, Douwe ^b,c   Teusink, Bas ^b,c   Versalovic, James ^a,d  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^d TEXAS CHILDREN S HOSPITAL   (United States)

^e SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL ENZYME; BINDING PROTEIN; CYANOCOBALAMIN; EXOPOLYSACCHARIDE; FOLIC ACID; PROBIOTIC AGENT; SCAVENGER; THIAMINE; POLYSACCHARIDE; TRANSCRIPTOME;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BIOFILM; BREAST MILK; CONTROLLED STUDY; GASTROINTESTINAL TRACT; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE SEQUENCE; IMMUNOMODULATION; LACTOBACILLUS REUTERI; MICROARRAY ANALYSIS; MUCUS; NONHUMAN; OPERON; PROTEIN SYNTHESIS; SEQUENCE HOMOLOGY; BACTERIUM ADHERENCE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; SPECIES DIFFERENCE;

LACTOBACILLUS REUTERI;

BACTERIAL ADHESION; BIOFILMS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HUMANS; LACTOBACILLUS REUTERI; METABOLIC NETWORKS AND PATHWAYS; MILK, HUMAN; MULTIGENE FAMILY; POLYSACCHARIDES; PROBIOTICS; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 79955718307     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018783     Document Type: Article

References (80)

1. Nelson KE, Weinstock GM, Highlander SK, Worley KC, Creasy HH, et al. (2010) A catalog of reference genomes from the human microbiome. Science 328: 994-999.
2. 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.
3. Reuter G, (2001) The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Curr Issues Intest Microbiol 2: 43-53.
4. Abrahamsson TR, Sinkiewicz G, Jakobsson T, Fredrikson M, Bjorksten B, (2009) Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J Pediatr Gastroenterol Nutr 49: 349-354.
5. Walter J, Britton RA, Roos S, (2010) Microbes and Health Sackler Colloquium: Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A In Press.
6. Oh PL, Benson AK, Peterson DA, Patil PB, Moriyama EN, et al. (2010) Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J 4: 377-387.
7. FAO/WHO (2001) Evaluation of health and nutritional properties of probiotics in food, including powder milk with live lactic acid bacteria. Food and Agricultural Organization of United Nations and World Health Organization Expert Consultation Report, London, Ontario, Canada.
8. Rosander A, Connolly E, Roos S, (2008) Removal of antibiotic resistance gene-carrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Appl Environ Microbiol 74: 6032-6040.
9. Savino F, Pelle E, Palumeri E, Oggero R, Miniero R, (2007) Lactobacillus reuteri (American Type Culture Collection Strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study. Pediatrics 119: e124-130.
10. Indrio F, Riezzo G, Raimondi F, Bisceglia M, Cavallo L, et al. (2008) The effects of probiotics on feeding tolerance, bowel habits, and gastrointestinal motility in preterm newborns. J Pediatr 152: 801-806.
11. Coccorullo P, Strisciuglio C, Martinelli M, Miele E, Greco L, et al. (2010) Lactobacillus reuteri (DSM 17938) in Infants with Functional Chronic Constipation: A Double-Blind, Randomized, Placebo-Controlled Study. J Pediatr 157: 598-602.
12. Miniello VL, Brunetti L, Tesse R, Natile M, Armenio L, et al. (2010) Lactobacillus reuteri modulates cytokines production in exhaled breath condensate of children with atopic dermatitis. J Pediatr Gastroenterol Nutr 50: 573-576.
13. Jones SE, Versalovic J, (2009) Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol 9: 35.
14. Eaton KA, Honkala A, Auchtung TA, Britton RA, (2010) Probiotic Lactobacillus reuteri ameliorates disease due to Enterohemorrhagic Escherichia coli in germ free mice. Infect Immun In Press.
15. Talarico TL, Casas IA, Chung TC, Dobrogosz WJ, (1988) Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob Agents Chemother 32: 1854-1858.
16. Iyer C, Kosters A, Sethi G, Kunnumakkara AB, Aggarwal BB, et al. (2008) Probiotic Lactobacillus reuteri promotes TNF-induced apoptosis in human myeloid leukemia-derived cells by modulation of NF-kappaB and MAPK signalling. Cell Microbiol 10: 1442-1452.
17. Lin YP, Thibodeaux CH, Pena JA, Ferry GD, Versalovic J, (2008) Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm Bowel Dis 14: 1068-1083.
18. Spinler JK, Taweechotipatr M, Rognerud CL, Ou CN, Tumwasorn S, et al. (2008) Human-derived probiotic Lactobacillus reuteri demonstrate antimicrobial activities targeting diverse enteric bacterial pathogens. Anaerobe 14: 166-171.
19. Ventura M, O'Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, et al. (2009) Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7: 61-71.
20. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F, et al. (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A 105: 18964-18969.
21. Morita H, Toh H, Fukuda S, Horikawa H, Oshima K, et al. (2008) Comparative genome analysis of Lactobacillus reuteri and Lactobacillus fermentum reveal a genomic island for reuterin and cobalamin production. DNA Res 15: 151-161.
22. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, et al. (2009) Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human- mucus binding protein. Proc Natl Acad Sci U S A 106: 17193-17198.
23. Tettelin H, Masignani V, Cieslewicz MJ, Eisen JA, Peterson S, et al. (2002) Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Sci U S A 99: 12391-12396.
24. Molenaar D, Bringel F, Schuren FH, de Vos WM, Siezen RJ, et al. (2005) Exploring Lactobacillus plantarum genome diversity by using microarrays. J Bacteriol 187: 6119-6127.
25. Colijn C, Brandes A, Zucker J, Lun DS, Weiner B, et al. (2009) Interpreting expression data with metabolic flux models: predicting Mycobacterium tuberculosis mycolic acid production. PLoS Comput Biol 5: e1000489.
26. van Baarlen P, Troost FJ, van Hemert S, van der Meer C, de Vos WM, et al. (2009) Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci U S A 106: 2371-2376.
27. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, et al. (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103: 15611-15616.
28. Arskold E, Lohmeier-Vogel E, Cao R, Roos S, Radstrom P, et al. (2008) Phosphoketolase pathway dominates in Lactobacillus reuteri ATCC 55730 containing dual pathways for glycolysis. J Bacteriol 190: 206-212.
29. Obradors N, Badia J, Baldoma L, Aguilar J, (1988) Anaerobic metabolism of the L-rhamnose fermentation product 1,2-propanediol in Salmonella typhimurium. J Bacteriol 170: 2159-2162.
30. Crow VL, Thomas TD, (1982) Arginine metabolism in lactic streptococci. J Bacteriol 150: 1024-1032.
31. Corfield AP, Myerscough N, Longman R, Sylvester P, Arul S, et al. (2000) Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease. Gut 47: 589-594.
32. Rojas M, Ascencio F, Conway PL, (2002) Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Appl Environ Microbiol 68: 2330-2336.
33. Roos S, Aleljung P, Robert N, Lee B, Wadstrom T, et al. (1996) A collagen binding protein from Lactobacillus reuteri is part of an ABC transporter system? FEMS Microbiol Lett 144: 33-38.
34. Preidis GA, Hill C, Guerrant RL, Ramakrishna BS, Tannock GW, et al. (2011) Probiotics, Enteric, and Diarrheal Diseases, and Global Health. Gastroenterology (In Press).
35. Young VR, (1994) Adults amino acids requirements: the case for a major revisions in current recommendations. The Journal of Nutrition 124: S1517-S1523.
36. Imura K, Okada A, (1998) Amino acid metabolism in pediatric patients. Nutrition 14: 143-148.
37. WHO Protein and amino acid requirements in human nutrition. pp. 265.
38. Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, et al. (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72: 3593-3599.
39. Scheppach W, (1994) Effects of short chain fatty acids on gut morphology and function. Gut 35: S35-38.
40. Bohle LA, Brede DA, Diep DB, Holo H, Nes IF, (2010) The mucus adhesion promoting protein (MapA) of Lactobacillus reuteri is specifically degraded to an antimicrobial peptide. Appl Environ Microbiol 76: 7306-7309.
41. Lebeer S, Verhoeven TL, Francius G, Schoofs G, Lambrichts I, et al. (2009) Identification of a Gene Cluster for the Biosynthesis of a Long, Galactose-Rich Exopolysaccharide in Lactobacillus rhamnosus GG and Functional Analysis of the Priming Glycosyltransferase. Appl Environ Microbiol 75: 3554-3563.
42. Bath K, Roos S, Wall T, Jonsson H, (2005) The cell surface of Lactobacillus reuteri ATCC 55730 highlighted by identification of 126 extracellular proteins from the genome sequence. FEMS Microbiol Lett 253: 75-82.
43. Stalhammar-Carlemalm M, Areschoug T, Larsson C, Lindahl G, (1999) The R28 protein of Streptococcus pyogenes is related to several group B streptococcal surface proteins, confers protective immunity and promotes binding to human epithelial cells. Mol Microbiol 33: 208-219.
44. Szajewska H, (2010) Can we trust meta-analysis on probiotics? Probiotics Watch. Danone Health Affairs. Paris, France 1: 2-3.
45. Pal C, Papp B, Lercher MJ, (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37: 1372-1375.
46. Iwasaki W, Takagi T, (2009) Rapid pathway evolution facilitated by horizontal gene transfers across prokaryotic lineages. PLoS Genet 5: e1000402.
47. Kaneuchi C, Seki M, Komagata K, (1988) Production of Succinic Acid from Citric Acid and Related Acids by Lactobacillus Strains. Appl Environ Microbiol 54: 3053-3056.
48. Hoppe B, Roth B, Bauerfeld C, Langman CB, (1998) Oxalate, citrate, and sulfate concentration in human milk compared with formula preparations: influence on urinary anion excretion. J Pediatr Gastroenterol Nutr 27: 383-386.
49. Whitehead K, Versalovic J, Roos S, Britton RA, (2008) Genomic and genetic characterization of the bile stress response of probiotic Lactobacillus reuteri ATCC 55730. Appl Environ Microbiol 74: 1812-1819.
50. Sinkiewicz G, Ljunggren L, (2008) Occurrence of Lactobacillus reuteri in human breast milk. Microb Ecol Health Disease 20: 122-126.
51. Miyoshi Y, Okada S, Uchimura T, Satoh E, (2006) A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Biosci Biotechnol Biochem 70: 1622-1628.
52. Mazmanian SK, Liu G, Jensen ER, Lenoy E, Schneewind O, (2000) Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc Natl Acad Sci U S A 97: 5510-5515.
53. van Pijkeren JP, Canchaya C, Ryan KA, Li Y, Claesson MJ, et al. (2006) Comparative and functional analysis of sortase-dependent proteins in the predicted secretome of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72: 4143-4153.
54. Coyne MJ, Chatzidaki-Livanis M, Paoletti LC, Comstock LE, (2008) Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis. Proc Natl Acad Sci U S A 105: 13099-13104.
55. Savage DC, (1986) Gastrointestinal microflora in mammalian nutrition. Annu Rev Nutr 6: 155-178.
56. Santos F, (2008) Vitamin B12 synthesis in Lactobacillus reuteri Wageningen Wageningen University.
57. Santos F, Vera JL, van der Heijden R, Valdez G, de Vos WM, et al. (2008) The complete coenzyme B12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098. Microbiology 154: 81-93.
58. Begley TP, Downs DM, Ealick SE, McLafferty FW, Van Loon AP, et al. (1999) Thiamin biosynthesis in prokaryotes. Arch Microbiol 171: 293-300.
59. Metges CC, (2000) Contribution of microbial amino acids to amino acid homeostasis of the host. J Nutr 130: 1857S-1864S.
60. Bartholome AL, Albin DM, Baker DH, Holst JJ, Tappenden KA, (2004) Supplementation of total parenteral nutrition with butyrate acutely increases structural aspects of intestinal adaptation after an 80% jejunoileal resection in neonatal piglets. JPEN J Parenter Enteral Nutr 28: 210-222 discussion 222-213.
61. Axelson LT, Chung TC, Dobrogosz WJ, Lindgren SE, (1989) Production of a broad antimicrobial substance by Lactobacillus reuteri. Microb Ecol Health Disease 2: 131-136.
62. Thomas CM, Versalovic J, (2010) Probiotics-host communication: Modulation of signaling pathways in the intestine. Gut Microbes 1: 1-16.
63. Peant B, LaPointe G, Gilbert C, Atlan D, Ward P, et al. (2005) Comparative analysis of the exopolysaccharide biosynthesis gene clusters from four strains of Lactobacillus rhamnosus. Microbiology 151: 1839-1851.
64. Yasuda E, Serata M, Sako T, (2008) Suppressive effect on activation of macrophages by Lactobacillus casei strain Shirota genes determining the synthesis of cell wall-associated polysaccharides. Appl Environ Microbiol 74: 4746-4755.
65. Lamothe GT, Jolly L, Mollet B, Stingele F, (2002) Genetic and biochemical characterization of exopolysaccharide biosynthesis by Lactobacillus delbrueckii subsp. bulgaricus. Arch Microbiol 178: 218-228.
66. Chabot S, Yu H, De Leselec L, Cloutier D, Van Calsteren M, et al. (2001) Exopolysaccharides from Lactobacillus rhamnosus RW-9595M stimulate TNF, IL-6 and IL-12 in human and mouse cultured immunocompetent cells, and IFN gamma in mouse splenocytes. Lait 81: 683-687.
67. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, et al. The integrated microbial genomes system: an expanding comparative analysis resource. Nucleic Acids Res 38: D382-390.
68. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
69. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-288.
70. Selengut JD, Haft DH, Davidsen T, Ganapathy A, Gwinn-Giglio M, et al. (2007) TIGRFAMs and Genome Properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res 35: D260-264.
71. Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al. (2005) InterPro, progress and status in 2005. Nucleic Acids Res 33: D201-205.
72. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
73. Notebaart RA, van Enckevort FH, Francke C, Siezen RJ, Teusink B, (2006) Accelerating the reconstruction of genome-scale metabolic networks. BMC Bioinformatics 7: 296.
74. Teusink B, Wiersma A, Molenaar D, Francke C, de Vos WM, et al. (2006) Analysis of growth of Lactobacillus plantarum WCFS1 on a complex medium using a genome-scale metabolic model. J Biol Chem 281: 40041-40048.
75. Oliveira AP, Nielsen J, Forster J, (2005) Modeling Lactococcus lactis using a genome-scale flux model. BMC Microbiol 5: 39.
76. Oh YK, Palsson BO, Park SM, Schilling CH, Mahadevan R, (2007) Genome-scale reconstruction of metabolic network in Bacillus subtilis based on high-throughput phenotyping and gene essentiality data. J Biol Chem 282: 28791-28799.
77. Reed JL, Vo TD, Schilling CH, Palsson BO, (2003) An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol 4: R54.
78. O'Brien KP, Remm M, Sonnhammer EL, (2005) Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res 33: D476-480.
79. Saulnier DM, Gibson GR, Kolida S, (2008) In vitro effects of selected synbiotics on the human faecal microbiota composition. FEMS Microbiol Ecol 66: 516-527.
80. Wall T, Bath K, Britton RA, Jonsson H, Versalovic J, et al. (2007) The early response to acid shock in Lactobacillus reuteri involves the ClpL chaperone and a putative cell wall-altering esterase. Appl Environ Microbiol 73: 3924-3935.