Symbiosis, dysbiosis, and rebiosis-The value of metaproteomics in human microbiome monitoring

Proteomics

Volumn 15, Issue 5-6, 2015, Pages 1142-1151

  Mao, Lei ^a   Franke, Jacqueline ^a  

^a UNIVERSITY OF APPLIED SCIENCES   (Germany)

Author keywords

Complex biomarkers; Dysbiosis; Gut microbiome; Metaproteomics; Preventive medicine; System biology

Indexed keywords

ANTIBIOTIC AGENT; BIOLOGICAL MARKER; POLYSACCHARIDE; PROTEIN;

BACTERIA; BACTERIAL VIRULENCE; CROHN DISEASE; DYSBIOSIS; ECOSYSTEM; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; METAGENOMICS; METAPROTEOMICS; MICROBIOME; MICROORGANISM; MONITORING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEOMICS; PROTOZOON; QUORUM SENSING; REBIOSIS; REVIEW; RISK; SYMBIOSIS; SYSTEMS BIOLOGY; ULCERATIVE COLITIS; YEAST; MICROFLORA; PROCEDURES;

BIOMARKERS; DYSBIOSIS; HUMANS; METAGENOMICS; MICROBIOTA; PROTEOMICS; SYMBIOSIS; SYSTEMS BIOLOGY;

EID: 84924714721     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400329     Document Type: Review

References (95)

1. Bjornerud, M., Reading the Rocks: The Autobiography of the Earth, Basic Books 2005. Available at http://www.amazon.com/Reading-Rocks-The-Autobiography-Earth/dp/0465006841.
2. Bidle, K. D., Lee, S., Marchant, D. R., Falkowski, P. G., Fossil genes and microbes in the oldest ice on earth. Proc. Natl. Acad. Sci. USA 2007, 104, 13455-13460.
3. Javaux, E. J., Knoll, A. H., Walter, M., Recognizing and interpreting the fossils of early eukaryotes. Orig. Life Evol. Biosph. 2003, 33, 75-94.
4. Gevers, D., Knight, R., Petrosino, J. F., Huang, K. et al., The Human Microbiome Project: a community resource for the healthy human microbiome. PLoS Biol. 2012, 10, e1001377.
5. Relman, D. A., Restoration of the gut microbial habitat as a disease therapy. Nat. Biotechnol. 2013, 31, 35-37.
6. Woese, C. R., Fox, G. E., Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl. Acad. Sci. USA 1977, 74, 5088-5090.
7. Pace, N. R., Sapp, J., Goldenfeld, N., Phylogeny and beyond: scientific, historical, and conceptual significance of the first tree of life. Proc. Natl. Acad. Sci. USA 2012, 109, 1011-1018.
8. Wilmes, P., Bond, P. L., The application of two-dimensional polyacrylamide gel electrophoresis and downstream analyses to a mixed community of prokaryotic microorganisms. Environ. Microbiol. 2004, 6, 911-920.
9. Handelsman, J., Rondon, M. R., Brady, S. F., Clardy, J. et al., Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 1998, 5, R245-R249.
10. Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L. et al., Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004, 304, 66-74.
11. Tanca, A., Palomba, A., Deligios, M., Cubeddu, T. et al., Evaluating the impact of different sequence databases on metaproteome analysis: insights from a lab-assembled microbial mixture. PLoS One 2013, 8, e82981.
12. Wilmes, P., Bond, P. L., Microbial community proteomics: elucidating the catalysts and metabolic mechanisms that drive the Earth's biogeochemical cycles. Curr. Opin. Microbiol. 2009, 12, 310-317.
13. Washburn, M. P., Wolters, D., Yates, J. R. 3rd, Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19, 242-247.
14. Verberkmoes, N. C., Russell, A. L., Shah, M., Godzik, A. et al., Shotgun metaproteomics of the human distal gut microbiota. Isme J. 2009, 3, 179-189.
15. Gil, R., Silva, F. J., Pereto, J., Moya, A., Determination of the core of a minimal bacterial gene set. Microbiol. Mol. Biol. Rev. 2004, 68, 518-537.
16. Rooijers, K., Kolmeder, C., Juste, C., Dore, J. et al., An iterative workflow for mining the human intestinal metaproteome. BMC Genomics 2011, 12, 6.
17. Ram, R. J., Verberkmoes, N. C., Thelen, M. P., Tyson, G. W. et al., Community proteomics of a natural microbial biofilm. Science 2005, 308, 1915-1920.
18. Lo, I., Denef, V. J., Verberkmoes, N. C., Shah, M. B. et al., Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 2007, 446, 537-541.
19. Wilmes, P., Wexler, M., Bond, P. L., Metaproteomics provides functional insight into activated sludge wastewater treatment. PLoS One 2008, 3, e1778.
20. Mahowald, M. A., Rey, F. E., Seedorf, H., Turnbaugh, P. J. et al., Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc. Natl. Acad. Sci USA 2009, 106, 5859-5864.
21. Gill, S. R., Pop, M., Deboy, R. T., Eckburg, P. B. et al., Metagenomic analysis of the human distal gut microbiome. Science 2006, 312, 1355-1359.
22. Klaassens, E. S., de Vos, W. M., Vaughan, E. E., Metaproteomics approach to study the functionality of the microbiota in the human infant gastrointestinal tract. Appl. Environ. Microbiol. 2007, 73, 1388-1392.
23. Markowitz, V. M., Chen, I. M., Chu, K., Szeto, E. et al., IMG/M-HMP: a metagenome comparative analysis system for the Human Microbiome Project. PLoS One 2012, 7, e40151.
24. Ottman, N., Smidt, H., de Vos, W. M., Belzer, C., The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol. 2012, 2, 104.
25. Qin, J., Li, R., Raes, J., Arumugam, M. et al., A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464, 59-65.
26. Kinross, J. M., Darzi, A. W., Nicholson, J. K., Gut microbiome-host interactions in health and disease. Genome Med. 2011, 3, 14.
27. Garrido, D., Barile, D., Mills, D. A., A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract. Adv. Nutr. 2012, 3, 415S-421S.
28. McFall-Ngai, M., Hadfield, M. G., Bosch, T. C., Carey, H. V. et al., Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 2013, 110, 3229-3236.
29. Gibson, G. R., Wang, X., Enrichment of bifidobacteria from human gut contents by oligofructose using continuous culture. FEMS Microbiol. Lett. 1994, 118, 121-127.
30. Bry, L., Falk, P. G., Midtvedt, T., Gordon, J. I., A model of host-microbial interactions in an open mammalian ecosystem. Science 1996, 273, 1380-1383.
31. Roos, S., Dicksved, J., Tarasco, V., Locatelli, E. et al., 454 pyrosequencing analysis on faecal samples from a randomized DBPC trial of colicky infants treated with Lactobacillus reuteri DSM 17938. PLoS One 2013, 8, e56710.
32. Bergstrom, A., Skov, T. H., Bahl, M. I., Roager, H. M. et al., Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl. Environ. Microbiol. 2014, 80, 2889-2900.
33. Eggesbo, M., Moen, B., Peddada, S., Baird, D. et al., Development of gut microbiota in infants not exposed to medical interventions. Apmis 2011, 119, 17-35.
34. Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A. et al., Development of the human infant intestinal microbiota. PLoS Biol. 2007, 5, e177.
35. Scholtens, P. A., Oozeer, R., Martin, R., Amor, K. B. et al., The early settlers: intestinal microbiology in early life. Annu. Rev. Food Sci. Technol. 2012, 3, 425-447.
36. Li, X., LeBlanc, J., Truong, A., Vuthoori, R. et al., A metaproteomic approach to study human-microbial ecosystems at the mucosal luminal interface. PLoS One 2011, 6, e26542.
37. Rehman, A., Lepage, P., Nolte, A., Hellmig, S. et al., Transcriptional activity of the dominant gut mucosal microbiota in chronic inflammatory bowel disease patients. J. Med. Microbiol. 2010, 59, 1114-1122.
38. Reigstad, C. S., Kashyap, P. C., Beyond phylotyping: understanding the impact of gut microbiota on host biology. Neurogastroenterol. Motil. 2013, 25, 358-372.
39. Pflughoeft, K. J., Versalovic, J., Human microbiome in health and disease. Annu. Rev. Pathol. 2012, 7, 99-122.
40. Moreira, C. G., Sperandio, V., Interplay between the QseC and QseE bacterial adrenergic sensor kinases in Salmonella enterica serovar Typhimurium pathogenesis. Infect Immun. 2012, 80, 4344-4353.
41. Abreu, M. T., Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat. Rev. Immunol. 2010, 10, 131-144.
42. Stappenbeck, T. S., Hooper, L. V., Gordon, J. I., Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 2002, 99, 15451-15455.
43. Masuda, K., Nakamura, K., Yoshioka, S., Fukaya, R. et al., Regulation of microbiota by antimicrobial peptides in the gut. Adv. Otorhinolaryngol. 2011, 72, 97-99.
44. Haller, D., Bode, C., Hammes, W. P., Pfeifer, A. M. et al., Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 2000, 47, 79-87.
45. Tracey, K. J., Cerami, A., Tumor necrosis factor, other cytokines and disease. Annu. Rev. Cell Biol. 1993, 9, 317-343.
46. Bouskra, D., Brezillon, C., Berard, M., Werts, C. et al., Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008, 456, 507-510.
47. Heumann, D., Barras, C., Severin, A., Glauser, M. P. et al., Gram-positive cell walls stimulate synthesis of tumor necrosis factor alpha and interleukin-6 by human monocytes. Infect Immun. 1994, 62, 2715-2721.
48. Miettinen, M., Vuopio-Varkila, J., Varkila, K., Production of human tumor necrosis factor alpha, interleukin-6, and interleukin-10 is induced by lactic acid bacteria. Infect Immun. 1996, 64, 5403-5405.
49. Tang, Y., Underwood, A., Gielbert, A., Woodward, M. J. et al., Metaproteomics analysis reveals the adaptation process for the chicken gut microbiota. Appl. Environ. Microbiol. 2014, 80, 478-485.
50. de Almeida, A. M., Bendixen, E., Pig proteomics: a review of a species in the crossroad between biomedical and food sciences. J. Proteomics 2012, 75, 4296-4314.
51. Cabreiro, F., Gems, D., Worms need microbes too: microbiota, health and aging in Caenorhabditis elegans. EMBO Mol. Med. 2013, 5, 1300-1310.
52. Gratacap, R. L., Wheeler, R. T., Utilization of zebrafish for intravital study of eukaryotic pathogen-host interactions. Dev. Comp. Immunol. 2014, 46, 108-115.
53. Human_Microbiome_Project_Consortium, A framework for human microbiome research. Nature 2012, 486, 215-221.
54. Kolmeder, C. A., de Vos, W. M., Metaproteomics of our microbiome-developing insight in function and activity in man and model systems. J. Proteomics 2014, 97, 3-16.
55. Karlsson, F., Tremaroli, V., Nielsen, J., Backhed, F., Assessing the human gut microbiota in metabolic diseases. Diabetes 2013, 62, 3341-3349.
56. Schneider, T., Riedel, K., Environmental proteomics: analysis of structure and function of microbial communities. Proteomics 2010, 10, 785-798.
57. Korecka, A., Arulampalam, V., The gut microbiome: scourge, sentinel or spectator? J. Oral. Microbiol. 2012, 4, 21.
58. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D. et al., Enterotypes of the human gut microbiome. Nature 2011, 473, 174-180.
59. Robles-Alonso, V., Guarner, F., Progress in the knowledge of the intestinal human microbiota. Nutr. Hosp. 2013, 28, 553-557.
60. David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B. et al., Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559-563.
61. De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M. et al., Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107, 14691-14696.
62. Ou, J., Carbonero, F., Zoetendal, E. G., DeLany, J. P. et al., Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am. J. Clin. Nutr. 2013, 98, 111-120.
63. Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I. et al., Human gut microbiome viewed across age and geography. Nature 2012, 486, 222-227.
64. Backhed, F., Ding, H., Wang, T., Hooper, L. V. et al., The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 2004, 101, 15718-15723.
65. Macfarlane, G. T., Cummings, J. H., Allison, C., Protein degradation by human intestinal bacteria. J. Gen. Microbiol. 1986, 132, 1647-1656.
66. Scott, K. P., Gratz, S. W., Sheridan, P. O., Flint, H. J. et al., The influence of diet on the gut microbiota. Pharmacol. Res. 2013, 69, 52-60.
67. Shoaie, S., Nielsen, J., Elucidating the interactions between the human gut microbiota and its host through metabolic modeling. Front Genet. 2014, 5, 86.
68. Ley, R. E., Backhed, F., Turnbaugh, P., Lozupone, C. A. et al., Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA 2005, 102, 11070-11075.
69. Hooper, L. V., Gordon, J. I., Commensal host-bacterial relationships in the gut. Science 2001, 292, 1115-1118.
70. Sonnenburg, E. D., Zheng, H., Joglekar, P., Higginbottom, S. K. et al., Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 2010, 141, 1241-1252.
71. Vijay-Kumar, M., Aitken, J. D., Carvalho, F. A., Cullender, T. C. et al., Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 2010, 328, 228-231.
72. Hoffner, K., Harwood, S.M, Barton, P. I., A reliable simulator for dynamic flux balance analysis. Biotechnol. Bioeng. 2013, 110, 792-802.
73. Khandelwal, R. A., Olivier, B. G., Roling, W. F., Teusink, B. et al., Community flux balance analysis for microbial consortia at balanced growth. PLoS One 2013, 8, e64567.
74. Rosenstiel, P., Stories of love and hate: innate immunity and host-microbe crosstalk in the intestine. Curr. Opin. Gastroenterol. 2013, 29, 125-132.
75. Schreiber, S., Rosenstiel, P., Albrecht, M., Hampe, J. et al., Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat. Rev. Genet. 2005, 6, 376-388.
76. Khan, K. J., Ullman, T. A., Ford, A. C., Abreu, M. T. et al., Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am. J. Gastroenterol. 2011, 106, 661-673.
77. Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K. et al., Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006, 55, 205-211.
78. Jones, M. L., Martoni, C. J., Ganopolsky, J. G., Labbe, A. et al., The human microbiome and bile acid metabolism: dysbiosis, dysmetabolism, disease and intervention. Expert Opin. Biol. Ther. 2014, 14, 467-482.
79. Smillie, C. S., Smith, M. B., Friedman, J., Cordero, O. X. et al., Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011, 480, 241-244.
80. Erickson, A. R., Cantarel, B. L., Lamendella, R., Darzi, Y. et al., Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn's disease. PLoS One 2012, 7, e49138.
81. Freiwald, A., Mao, L., Kodelja, V., Kliem, M. et al., Differential analysis of Crohn's disease and ulcerative colitis by mass spectrometry. Inflamm Bowel Dis. 2011, 17, 1051-1052.
82. Mao, L., Stafforst, T., Kuepfer, L., Olbrich, C. et al., Gesundheit, in: Biotechnologie, Z. (Ed.), Dechema Diskussionspaper "Biotechnologie - der Schlüssel zur Bioökonomie". Dechema: Frankfurt M 2014.
83. Putignani, L., Del Chierico, F., Petrucca, A., Vernocchi, P. et al., The human gut microbiota: a dynamic interplay with the host from birth to senescence settled during childhood. Pediatr. Res. 2014, 76, 2-10.
84. Del Chierico, F., Vernocchi, P., Bonizzi, L., Carsetti, R. et al., Early-life gut microbiota under physiological and pathological conditions: the central role of combined meta-omics-based approaches. J. Proteomics 2012, 75, 4580-4587.
85. Jansson, J. K., Neufeld, J. D., Moran, M. A., Gilbert, J. A., Omics for understanding microbial functional dynamics. Environ. Microbiol. 2012, 14, 1-3.
86. Zarraonaindia, I., Smith, D. P., Gilbert, J. A., Beyond the genome: community-level analysis of the microbial world. Biol. Philos. 2013, 28, 261-282.
87. Munoz-Tamayo, R., Laroche, B., Walter, E., Dore, J. et al., Mathematical modelling of carbohydrate degradation by human colonic microbiota. J. Theor. Biol. 2010, 266, 189-201.
88. Thiele, I., Fleming, R. M., Que, R., Bordbar, A. et al., Multiscale modeling of metabolism and macromolecular synthesis in E. coli and its application to the evolution of codon usage. PLoS One 2012, 7, e45635.
89. Shoaie, S., Karlsson, F., Mardinoglu, A., Nookaew, I. et al., Understanding the interactions between bacteria in the human gut through metabolic modeling. Sci. Rep. 2013, 3, 2532.
90. Heinken, A., Sahoo, S., Fleming, R. M., Thiele, I., Systems-level characterization of a host-microbe metabolic symbiosis in the mammalian gut. Gut Microbes 2013, 4, 28-40.
91. Bucci, V., Xavier, J. B., Towards predictive models of the human gut microbiome. J. Mol. Biol. 2014, 2836, 00178-8.
92. Greenblum, S., Turnbaugh, P. J., Borenstein, E., Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc. Natl. Acad. Sci. USA 2012, 109, 594-599.
93. Jehmlich, N., Schmidt, F., von Bergen, M., Richnow, H. H. et al., Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures. Isme J. 2008, 2, 1122-1133.
94. Pan, C., Fischer, C. R., Hyatt, D., Bowen, B. P. et al., Quantitative tracking of isotope flows in proteomes of microbial communities. Mol. Cell Proteomics 2011, 10, M110 006049.
95. Seifert, J., Taubert, M., Jehmlich, N., Schmidt, F. et al., Protein-based stable isotope probing (protein-SIP) in functional metaproteomics. Mass Spectrom. Rev. 2012, 31, 683-697.