Integrating '-omics' and natural product discovery platforms to investigate metabolic exchange in microbiomes

Current Opinion in Chemical Biology

Volumn 15, Issue 1, 2011, Pages 79-87

  Yang, Jane Y ^a   Karr, Jessica R ^a   Watrous, Jeramie D ^a   Dorrestein, Pieter C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; AUREUSIMINE; COLIBACTIN; ESTRADIOL; GLUCAGON LIKE PEPTIDE 1; MICROCOCIN B17; NATURAL PRODUCTS AND THEIR SYNTHETIC DERIVATIVES; NORADRENALIN; STAPHYLOXANTHIN; UNCLASSIFIED DRUG;

BACILLUS SUBTILIS; BIFIDOBACTERIUM LONGUM; BURKHOLDERIA; CANDIDA ALBICANS; CHEMICAL COMPOSITION; CLOSTRIDIUM; HELICOBACTER PYLORI; HUMAN; METABOLISM; METABOLOMICS; MICROBIOME; NONHUMAN; PEPTIDOMICS; PORPHYROMONAS GINGIVALIS; PROPIONIBACTERIUM FREUDENREICHII SHERMANII; PROTEOMICS; PSEUDOMONAS AERUGINOSA; REVIEW; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TREPONEMA DENTICOLA;

ANIMALS; BIOLOGICAL PRODUCTS; COMPUTATIONAL BIOLOGY; GENOMICS; HUMANS; METAGENOME;

EID: 79851507789     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2010.10.025     Document Type: Review

References (101)

1. Zaura E., Keijser B.J.F., Huse S.M., Crielaard W. Defining the healthy 'core microbiome' of oral microbial communities. BMC Microbiol 2009, 9:259.
2. Turnbaugh P.J., Quince C., Faith J.J., McHardy A.C., Yatsunenko T., Niazi F., Affourtit J., Egholm M., Henrissat B., Knight R., et al. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci U S A 2010, 107:7503-7508.
3. Crimmins E., Vasunilashorn S., Kim J.K., Alley D. Biomarkers related to aging in human populations. Adv Clin Chem 2008, Vol46:161-216.
4. Turnbaugh P.J., Ridaura V.K., Faith J.J., Rey F.E., Knight R., Gordon J.I. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009, 1:ra14.
5. Sartor R.B. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008, 134:577-594.
6. Fierer N., Hamady M., Lauber C.L., Knight R. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl AcadSciU SA 2008, 105:17994-17999.
7. Grice E.A., Kong H.H., Renaud G., Young A.C., Bouffard G.G., Blakesley R.W., Wolfsberg T.G., Turner M.L., Segre J.A., Nisc Comparative S. A diversity profile of the human skin microbiota. Genome Res 2008, 18:1043-1050.
8. Rawls J.F., Mahowald M.A., Goodman A.L., Trent C.M., Gordon J.I. In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proc Natl Acad Sci U S A 2007, 104:7622-7627.
9. Samuel B.S., Gordon J.I. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci U S A 2006, 103:10011-10016.
10. Martin F.P.J., Dumas M.E., Wang Y.L., Legido-Quigley C., Yap I.K.S., Tang H.R., Zirah S., Murphy G.M., Cloarec O., Lindon J.C., et al. A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model. Mol Syst Biol 2007, 3:112.
11. Hooper L.V., Gordon J.I. Commensal host-bacterial relationships in the gut. Science 2001, 292:1115-1118.
12. Burkholder P.R., McVeigh I. Synthesis of vitamins by intestinal bacteria. Proc Natl Acad Sci U S A 1942, 28:285-289.
13. Mazmanian S.K., Liu C.H., Tzianabos A.O., Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005, 122:107-118.
14. Mazmanian S.K., Round J.L., Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008, 453:620-625.
15. Palmer C., Bik E.M., DiGiulio D.B., Relman D.A., Brown P.O. Development of the human infant intestinal microbiota. PLoS Biol 2007, 5:1556-1573.
16. Ivanov I.I., Frutos R.D., Manel N., Yoshinaga K., Rifkin D.B., Sartor R.B., Finlay B.B., Littman D.R. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008, 4:337-349.
17. Thompson C.L., Hofer M.J., Campbell I.L., Holmes A.J. Community dynamics in the mouse gut microbiota: a possible role for IRF9-regulated genes in community homeostasis. PLoS One 2010, 5.
18. Mulder I.E., Schmidt B., Stokes C.R., Lewis M., Bailey M., Aminov R.I., Prosser J.I., Gill B.P., Pluske J.R., Mayer C.D., et al. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biol 2009, 7.
19. Lai Y.P., Di Nardo A., Nakatsuji T., Leichtle A., Yang Y., Cogen A.L., Wu Z.R., Hooper L.V., Schmidt R.R., von Aulock S., et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 2009, 15. 1377-U1374.
20. Salzman N.H., Hung K.C., Haribhai D., Chu H.T., Karlsson-Sjoberg J., Amir E., Teggatz P., Barman M., Hayward M., Eastwood D., et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010, 11. 76-U71.
21. Srikanth C.V., McCormick B.A. Interactions of the intestinal epithelium with the pathogen and the indigenous microbiota: a three-way crosstalk. Interdisciplinary Perspect Infect Dis 2008, 2008:626827.
22. Hattori M., Taylor T.D. The human intestinal microbiome: a new frontier of human biology. DNA Res 2009, 16:1-12.
23. Gallo R.L., Nizet V. Innate barriers against skin infection and associated disorders. Drug Discov Today: Dis Mech 2008, 5:e145-e152.
24. Clardy J., Fischbach M.A., Walsh C.T. New antibiotics from bacterial natural products. Nat Biotechnol 2006, 24:1541-1550.
25. Ruas-Madiedo P, Medrano M, Salazar N, De Los Reyes-Gavilan CG, Perez PF, Abraham AG: Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. J Appl Microbiol, doi:10.1111/j.1365-2672.2010.04839.x.
26. Al-Lahham S.H., Peppelenbosch M.P., Roelofsen H., Vonk R.J., Venema K. Biological effects of proprionic acid in humans; metabolism, potential applications and underlying mechanisms. Biochim Biophys Acta 2010, 1801:1175-1183.
27. Wei M.Q., Mengesha A., Good D., Anne J. Bacterial targeted tumor therapy-dawn of a new era. Cancer Lett 2008, 259:16-27.
28. Turroni F., Ribbera A., Foroni E., van Sinderen D., Ventura M. Human gut microbiota and bifidobacteria: from composition to functionality. Antonie Van Leeuwenhoek 2008, 94:35-50.
29. Frank D.N., Amand A.L.S., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007, 104:13780-13785.
30. Peterson D.A., Frank D.N., Pace N.R., Gordon J.I. Metagenomic approaches for defining the pathogenesis of inflammatory bowel diseases. Cell Host Microbe 2008, 3:417-427.
31. Son G., Kremer M., Hines I.N. Contribution of gut bacteria to liver pathobiology. Gastroenterol Res Pract 2010, 2010:13.
32. Peschel A., Sahl H.-G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 2006, 4:529-536.
33. Ley R.E., Peterson D.A., Gordon J.I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006, 124:837-848.
34. Giongo A., Gano K.A., Crabb D.B., Mukherjee N., Novelo L.L., Casella G., Drew J.C., Ilonen J., Knip M., Hyoty H., et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J 2010, 1-10.
35. Ley R.E. Obesity and the human microbiome. Curr Opin Gastroenterol 2010, 26:5-11.
36. Huffnagle G.B. The microbiota and allergies/asthma. PLoS Pathogens 2010, 6:e1000549.
37. Lampe J.W. The human microbiome project: getting to the guts of the matter in cancer epidemiology. Cancer Epidemiol Biomarkers Prevent 2008, 17:2523-2524.
38. San Millan J.L., Kolter R., Moreno F. Plasmid genes required for microcin B17 production. J Bacteriol 1985, 163:1016-1020.
39. Putze J., Hennequin C., Nougayrede J.-P., Zhang W., Homburg S., Karch H., Bringer M.-A., Fayolle C., Carniel E., Rabsch W., et al. Genetic structure and distribution of the colibactin genomic island among Enterobacteriaceae. Infect Immun 2009, 77:4696-4703.
40. Liu G.Y., Essex A., Buchanan J.T., Datta V., Hoffman H.M., Bastian J.F., Fierer J., Nizet V. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med 2005, 202:209-215.
41. Zimmerman M., Fischbach M. A Family of pyrazinone natural products from a conserved nonribosomal peptide synthetase in Staphylococcus aureus. Chem Biol 2010, 17:925-930.
42. Wyatt M.A., Wang W.L., Roux C.M., Beasley F.C., Heinrichs D.E., Dunman P.M., Magarvey N.A. Staphylococcus aureus nonribosomal peptide secondary metabolites regulate virulence. Science 2010, 329:294-296.
43. Hartman A.L., Lough D.M., Barupal D.K., Fiehn O., Fishbein T., Zasloff M., Eisen J.A. Human gut microbiome adopts an alternative state following small bowel transplantation. Proc Natl Acad Sci U S A 2009, 106:17187-17192.
44. Gonzalez D.J., Lee S.W., Hensler M.E., Markley A.L., Dahesh S., Mitchell D.A., Bandeira N., Nizet V., Dixon J.E., Dorrestein P.C. Clostridiolysin S, a post-translationally modified biotoxin from Clostridium botulinum. J Biol Chem 2010, 285:28220-28228.
45. Mocibob M, Ivic N., Bilokapic S., Maier T., Luic M., Ban N., Weygand-Durasevic I. From the cover: homologs of animoacyl-tRNA synthetases acylate carrier proteins and provide a link between ribosomal and nonribosomal peptide synthesis. Proc Natl Acad Sci U S A 2010, 107:14585-14590.
46. Boontham P., Robins A., Chandran P., Pritchard D., Camara M., Williams P., Chuthapisith S., McKechnie A., Rowlands B.J., Eremin O. Significant immunomodulatory effects of Pseudomonas aeruginosa quorum-sensing signal molecules: possible link in human sepsis. Clin Sci (Lond) 2008, 115:343-351.
47. Singh G., Wu B., Baek M., Camargo A., Nguyen A., Slusher N., Srinivasan R., Wiener-Kronish J., Lynch S. Secretion of Pseudomonas aeruginosa type III cytotoxins is dependent on pseudomonas quinolone signal concentration. Microb Pathogen 2010, 49:8.
48. Bjarnsholt T., Jensen P.O., Jakobsen T.H., Phipps R., Nielsen A.K., Rybtke M.T., Tolker-Nielsen T., Givskov M., Hoiby N., Ciofu O., et al. Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS One 2010, 5:e10115.
49. Kravchenko V.V., Kaufmann G.F., Mathison J.C., Scott D.A., Katz A.Z., Grauer D.C., Lehmann M., Meijler M.M., Janda K.D., Ulevitch R.J. Modulation of gene expression via disruption of NF-kappa B signaling by a bacterial small molecule. Science 2008, 321:259-263.
50. Smith R.S., Fedyk E.R., Springer T.A., Mukaida N., Iglewski B.H., Phipps R.P. IL-8 production in human lung fibroblasts and epithelial cells activated by the Pseudomonas autoinducer N-3-oxododecanoyl homoserine lactone is transcriptionally regulated by NF-kappa B and activator protein-2. J Immunol 2001, 167:366-374.
51. Siezen R.J., Khayatt B.I. Natural products genomics. Microb Biotechnol 2008, 1:275-282.
52. Kunst F., Ogasawara N., Moszer I., Albertini A.M., Alloni G., Azevedo V., Bertero M.G., Bessieres P., Bolotin A., Borchert S., et al. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 1997, 390:249-256.
53. Lopez D., Kolter R. Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 2010, 34:134-149.
54. Fujiya M., Musch M.W., Nakagawa Y., Hu S., Alverdy J., Kohgo Y., Schneewind O., Jabri B., Chang E.B. The Bacillus subtilis quorum-sensing molecule CSF contributes to intestinal Homeostasis via OCTN2, a host cell membrane transporter. Cell Host Microbe 2007, 1:299-308.
55. Otto M., Echner H., Voelter W., Gotz F. Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 2001, 69:1957-1960.
56. Cogen A.L., Yamasaki K., Muto J., Sanchez K.M., Alexander L.C., Tanios J., Lai Y.P., Kim J.E., Nizet V., Gallo R.L. Staphylococcus epidermidis antimicrobial delta-toxin (Phenol-Soluble Modulin-gamma) cooperates with host antimicrobial peptides to kill group A Streptococcus. PLoS One 2010, 5:e8557.
57. Blaser M.J., Atherton J.C. Helicobacter pylori persistence: biology and disease. J Clin Invest 2004, 113:321-333.
58. Kiere D.A., Anton P., Faull K.F., Ruth E., Walsh J.H., Chew P., Quisimoro D., Territo M., Reeve J.R. Diethyl phthalate, a chemotactic factor secreted by Helicobacter pylori. J Biol Chem 2001, 276:48847-48853.
59. Uribe A, Alam M., Johansson O., Midtvedt T., Theodorsson E. Microflora modulates endocrine cells in the gastrointestinal mucosa of the rat. Gastroenterology 1994, 107:1259-1269.
60. Njoroge J., Sperandio V. Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Med 2009, 1:201-210.
61. Walters M., Sperandio V. Quorum sensing in Escherichia coli and Salmonella. Int JMed Microbiol 2006, 296:125-131.
62. Pentikainen V., Suomalainen L., Erkkila K., Martelin E., Parvinen M., Pentikainen M.O., Dunkel L. Nuclear factor-kB activation in human testicular apoptosis. Amer J Pathol 2002, 160:205-218.
63. Sonnex G. Influence of ovarian hormones on urogenital infection. Sexually Transmitted Infect 1998, 74:11-19.
64. Jahoor A., Williams S., Rumbaugh K. Microbial Signaling Compounds as Endocrine Effectors 2010, Springer, New York, NY. 1st edn. M. Lyte, P.P.E. Freestone (Eds.).
65. Fischbach M.A., Walsh C.T. Antibiotics for emerging pathogens. Science 2009, 325:1089-1093.
66. Walsh C.T., Acker M.G., Bowers A.A. Thiazolyl peptide antibiotic biosynthesis: a cascade of post-translational modifications on ribosomal nascent proteins. J Biol Chem 2010, 285:27525-27531.
67. Timmer A.M., Timmer J.C., Pence M.A., Hsu L.C., Ghochani M., Frey T.G., Karin M., Salvesen G.S., Nizet V. Streptolysin O promotes group A Streptococcus immune evastion by accelerated macrophage apoptosis. J Biol Chem 2009, 284:862-871.
68. Terada L.S., Johansen K.A., Nowbar S., Vasil A.I., Vasil M.L. Pseudomonas aeruginosa hemolytic phospholipase C suppresses neutrophil respiratory burst activity. Infect Immun 1999, 67:2371-2376.
69. Queck S.Y., Khan B.A., Wang R., Bach T.H., Kretschmer D., Chen L., Kreiswirth B.N., Peschel A., DeLeo F.R., Otto M. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. PLoS Pathogens 2009, 5:e1000533.
70. Molinski T.F. NMR of natural products at the 'nanomole-scale'. Nat Product Rep 2010, 27:321-329.
71. Schroeder F.C., Gibson D.M., Churchill A.C.L., Sojikul P., Wursthorn E.J., Krasnoff S.B., Clardy J. Differential analysis of 2D NMR spectra: new natural products from a pilot-scale fungal extract library. Angew Chem Int Ed 2007, 46:901-904.
72. Taggi A.E., Meinwald J., Schroeder F.C. A new approach to natural products discovery exemplified by the identification of sulfated nucleosides in spider venom. J Amer Chem Soc 2004, 126:10364-10369.
73. Dossey A.T., Walse S.S., Rocca J.R., Edison A.S. Single-insect NMR: a new tool to probe chemical biodiversity. ACS Chem Biol 2006, 1:511-514.
74. Exarchou V., Krucker M., van Beek T.A., Vervoort J., Gerothanassis I.P., Albert K. LC-NMR coupling technology: recent advancements and applications in natural products analysis. Magn Reson Chem 2005, 43:681-687.
75. Schroder F.C., Farmer J.J., Attygalle A.B., Smedley S.R., Eisner T., Meinwald J. Combinatorial chemistry in insects: a library of defensive macrocyclic polyamines. Science 1998, 281:428-431.
76. Cornett D.S., Reyzer M.L., Chaurand P., Caprioli R.M. MALDI imaging mass spectrometry: molecular snapshots of biochemical systems. Nat Methods 2007, 4:828-833.
77. Seeley E.H., Caprioli R.M. Molecular imaging of proteins in tissues by mass spectrometry. Proc Natl Acad Sci U S A 2008, 105:18126-18131.
78. Yang Y.L., Xu Y.Q., Straight P., Dorrestein P.C. Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol 2009, 5:885-887.
79. Liu W.-T., Julio Ng, Meluzzi D., Bandeira N., Gutierrez M., Simmons T.L., Schultz A.W., Linington R.G., Moore B.S., Gerwick W.H., et al. Interpretation of tandem mass spectra obtained from cyclic nonribosomal peptides. Anal Chem 2009, 81:4200-4209.
80. Bowen B.P., Northen T.R. Dealing with the unknown: metabolomics and metabolite atlases. J Amer Soc Mass Spectrom 2010, 21:1471-1476.
81. Jones B.V., Sun F.N., Marchesi J.R. Comparative metagenomic analysis of plasmid encoded functions in the human gut microbiome. BMC Genomics 2010, 11:46.
82. Pevzner P.A., Kim S., Ng J. Comment on 'protein sequences from mastodon and Tyrannosaurus rex revealed by mass spectrometry'. Science 2008, 321:1040.
83. Asara J.M., Schweitzer M.H., Freimark L.M., Phillips M., Cantley L.C. Protein sequences from mastodon and Tyrannosaurus rex revealed by mass spectrometry. Science 2007, 317:280-285.
84. Mitchell P. Proteomics retrenches. Nat Biotechnol 2010, 28:665-670.
85. Bandeira N., Tsur D., Frank A., Pevzner P.A. Protein identification by spectral networks analysis. Proc Natl Acad Sci U S A 2007, 104:6140-6145.
86. Wikoff W.R., Anfora A.T., Liu J., Schultz P.G., Lesley S.A., Peters E.C., Siuzdak G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 2009, 106:3698-3703.
87. Nicholson J.K., Wilson I.D. Understanding 'global' systems biology: metabonomics and the continuum of metabolism. Nat Rev Drug Discov 2003, 2:668-676.
88. Watrous J., Hendricks N., Meehan M., Dorrestein P.C. Capturing bacterial metabolic exchange using thin film desorption electrospray ionization-imaging mass spectrometry. Anal Chem 2010, 82:1598-1600.
89. Liu W.-T., Yang Y.-L., Xu Y., Lamsa A., Haste N.M., Yang J.Y., Ng J., Gonzalez D., Ellermeier C.D., Straight P.D., et al. Imaging mass spectrometry of intraspecies metabolic exchange revealed the cannibalistic factors of Bacillus subtilis. Proc Natl Acad Sci U S A 2010, 107:16286-16290.
90. Challis G.L. Mining microbial genomes for new natural products and biosynthetic pathways. Microbiology 2008, 154:1555-1569.
91. Li M.H.T., Ung P.M.U., Zajkowski J., Garneau-Tsodikova S., Sherman D.H. Automated genome mining for natural products. BMC Bioinformatics 2009, 10:185.
92. Atta-ur-Rahman, Choudhary M.I., Thomsen W.J. Bioassay Techniques for Drug Development 2001, Overseas Publishers Association, Amsterdam, The Netherlands.
93. Mazumdar V., Snitkin E.S., Amar S., Segre D. Metabolic network model of a human oral pathogen. JBacteriol 2009, 191:74-90.
94. Fischbach M.A., Krogan N.J. The next frontier of systems biology: higher-order and interspecies interactions. Genome Biol 2010, 11:208.
95. Nicholson J.K., Lindon J.C. Systems biology-metabonomics. Nature 2008, 455:1054-1056.
96. Ryan R.P., Fouhy Y., Lucey J.F., Dow J.M. Cyclic Di-GMP signaling in bacteria: recent advances and new puzzles. JBacteriol 2006, 188:8327-8334.
97. Kuramitsu H.K., Chen W., Ikegami A. Biofilm formation by the periodontopathic bacteria Treponema denticola and Porphyromonas gingivalis. J Periodontol 2005, 76:2047-2051.
98. Grenier D. Nutritional interactions between 2 suspected periodontopathogens, Treponema denticola and Porphyromonas gingivalis. Infect Immun 1992, 60:5298-5301.
99. Joyner PM, Liu J, Zhang Z, Merritt J, Fengxia Q, Cichewicz RH: Mutanobactin A from the human oral pathogen Streptococcus mutans is a cross-kingdom regulator of the yeast-mycelium transition. Org Biomol Chem 2010, advance article , Communication. doi:10.1039/C0OB00579G.
100. Yamazaki S., Kano K., Ikeda T., Isawa K., Kaneko T. Role of 2-amino-3-carboxy-1,4-naphthoquinone, a strong growth stimulator for bifidobacteria, as an electron transfer mediator for NAD(P)(+) regeneration in Bifidobacterium longum. Biochim Biophys Acta-Gen Subjects 1999, 1428:241-250.
101. Clayton T.A., Baker D., Lindon J.C., Everett J.R., Nicholson J.K. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc Natl Acad Sci U S A 2009, 106:14728-14733.