Agent based modeling of human gut microbiome interactions and perturbations

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Shashkova, Tatiana ^a,b   Popenko, Anna ^a   Tyakht, Alexander ^a   Peskov, Kirill ^c   Kosinsky, Yuri ^c   Bogolubsky, Lev ^d   Raigorodskii, Andrei ^d   Ischenko, Dmitry ^a   Alexeev, Dmitry ^a,b   Govorun, Vadim ^a  

^a FEDERAL RESEARCH AND CLINICAL CENTER OF PHYSICAL CHEMICAL MEDICINE OF FEDERAL MEDICAL BIOLOGICAL AGENCY   (Russian Federation)

^b MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^c M and S Decisions LLC   (Russian Federation)

^d YANDEX   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ANTIBIOTIC AGENT; BUTYRIC ACID; POLYSACCHARIDE; PROPIONIC ACID; ANTIINFECTIVE AGENT;

AGENT BASED MODEL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL MUTATION; BACTERIAL STRAIN; CONTROLLED STUDY; FERMENTATION; HUMAN; INTESTINE FLORA; MICROBIAL COMMUNITY; MODEL; NONHUMAN; ORGANISMAL INTERACTION; TREATMENT DURATION; ALGORITHM; BACTERIUM; BIOLOGICAL MODEL; DRUG EFFECTS; GENETICS; METABOLISM; MUTATION;

ALGORITHMS; ANTI-BACTERIAL AGENTS; BACTERIA; DRUG RESISTANCE, BACTERIAL; GASTROINTESTINAL MICROBIOME; HUMANS; MICROBIAL INTERACTIONS; MODELS, BIOLOGICAL; MUTATION;

EID: 84960970851     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148386     Document Type: Article

References (76)

1. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh Cet al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464: 59-65. doi: 10.1038/nature08821 PMID: 20203603
2. Consortium, H. M. P. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486: 207-14. doi: 10.1038/nature11234 PMID: 22699609
3. Lozupone C, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012; 489: 220-230. doi: 10.1038/nature11550 PMID: 22972295
4. Ley R.E., P. J, T. Microbial ecology: human gut microbes associated with obesity. Nature 2006; 444: 1022-1023. PMID: 17183309
5. Kau AL, Ahern PP, Griffin NW, Goodman AL, Jeffrey I. Human nutrition, the gut microbiome, and immune system: envisioning the future. Nature 2012; 474: 327-336.
6. Dicksved J, Halfvarson J, Rosenquist M, Järnerot G, Tysk C, Apajalahti J, et al. et al. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. ISME J. 2008; 2: 716-27. doi: 10.1038/ismej.2008.37 PMID: 18401439
7. Lupton J. R. Diet Induced Changes in the Colonic Environment and Colorectal Cancer Microbial Degradation Products Influence Colon Cancer Risk: the Butyrate Controversy. J. Nutr. 2004; 134: 479-482. PMID: 14747692
8. TyakhtA V, Kostryukova ES, Popenko AS, Belenikin MS, Pavlenko AV, Larin AK, et al. Human gut microbiota community structures in urban and rural populations in Russia. Nat. Commun. 2013; 4: 2469. doi: 10.1038/ncomms3469 PMID: 24036685
9. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012; 488: 178-84. doi: 10.1038/nature11319 PMID: 22797518
10. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A, et al. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 5859-64. doi: 10.1073/pnas.0901529106 PMID: 19321416
11. Davey ME, O'toole G. Microbial Biofilms: from Ecology to Molecular Genetics. Microbiol. Mol. Biol. Rev. 2000; 64: 847-867. PMID: 11104821
12. Moreira CG, Weinshenker D, Sperandio V. QseC mediates Salmonella entericaserovartyphimurium virulence in vitro and in vivo. Infect. Immun. 2010; 78: 914-26. doi: 10.1128/IAI.01038-09 PMID: 20028809
13. RheeSang H, Charalabos P, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiotaaxis. NIH Public Access 2013; 6.
14. Wintermute EH, Silver PA. Dynamics in the mixed microbial concourse. Genes Dev. 2010; 24: 2603-2614. doi: 10.1101/gad.1985210 PMID: 21123647
15. Nadell CD, Xavier JB, Foster KR. The sociobiology of biofilms. FEMS Microbiol. Rev. 2009; 33: 206-24. doi: 10.1111/j.1574-6976.2008.00150.x PMID: 19067751
16. Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, et al. Microbial co-occurrence relationships in the human microbiome. PLoSComput. Biol. 2012; 8: e1002606. doi: 10.1371/journal.pcbi.1002606 PMID: 22807668
17. Lidicker WZ. Clarification of interactions in ecological systems. 29, 475-477(1979).
18. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2004; 2: 95-108. PMID: 15040259
19. Seth EC, Taga ME. Nutrient cross-feeding in the microbial world. Front. Microbiol. 2014; 5: 350. doi: 10.3389/fmicb.2014.00350 PMID: 25071756
20. Levy R, Borenstein E. Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules. Proc. Natl. Acad. Sci. U. S.A. 2013; 110: 12804-9. doi: 10.1073/pnas.1300926110 PMID: 23858463
21. Li YH, Tian X. Quorum sensing and bacterial social interactions in biofilms. Sensors (Basel). 2012; 12: 2519-38.
22. Heinken A, Thiele I. Anoxic Conditions Promote Species-Specific Mutualism between Gut Microbes In Silico. Appl. Environ. Microbiol. 2015;' 81: 4049-61. doi: 10.1128/AEM.00101-15 PMID: 25841013
23. Cockrell C, Christley S, An G. Investigation of inflammation and tissue patterning in the gut using a Spatially Explicit General-purpose Model of Enteric Tissue (SEGMEnT). PLoSComput. Biol. 2014; 10: e1003507. doi: 10.1371/journal.pcbi.1003507 PMID: 24675765
24. Schluter J. & Foster K. R. The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol. 2012; 10: e1001424. doi: 10.1371/journal.pbio.1001424 PMID: 23185130
25. Marino S., Baxter N. T., Huffnagle G. B., Petrosino J. F. & Schloss P. D. Mathematical modeling of primary succession of murine intestinal microbiota. Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 439-44. doi: 10.1073/pnas.1311322111 PMID: 24367073
26. Scheuring I. &Yu D. W. How to assemble a beneficial microbiome in three easy steps. Ecol. Lett. 2012; 15: 1300-7. doi: 10.1111/j.1461-0248.2012.01853.x PMID: 22913725
27. An G. Introduction of an agent-based multi-scale modular architecture for dynamic knowledge representation of acute inflammation. Theor. Biol. Med. Model. 2008; 5:11. doi: 10.1186/1742-4682-5-11 PMID: 18505587
28. An G., Mi Q., Dutta-Moscato J. & Vodovotz Y. Agent-based models in translational systems biology. Wiley Interdiscip Rev Syst. Biuology Med. 2013; 1 (2): 156-171.
29. Frey E. Evolutionary game theory: Theoretical concepts and applications to microbial communities. Phys. A Stat. Mech. its Appl. 2010; 389: 4265-4298.
30. Stein RR, Bucci V, Toussaint NC, Buffie CG, Rätsch G, Pamer EG, et al. Ecological Modeling from Time-Series Inference: Insight into Dynamics and Stability of Intestinal Microbiota. PLoS Comput. Biol. 2013; 9: e1003388. doi: 10.1371/journal.pcbi.1003388 PMID: 24348232
31. Gore J., Youk H. & van Oudenaarden A. Snowdrift game dynamics and facultative cheating in yeast. Nature 2009; 459: 253-6. doi: 10.1038/nature07921 PMID: 19349960
32. May R. & Leonard W. Nonlinear aspects of competition between three species. SIAM J. Appl. Math. 1975; 29: 243-253.
33. Fernandes J., Su W., Rahat-Rozenbloom S., Wolever T. M. S. &Comelli E. M. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr. Diabetes 2014; 4: e121. doi: 10.1038/nutd.2014.23 PMID: 24979150
34. Dodd D., Moon Y.-H., Swaminathan K., Mackie R. I. & Cann I. K. O. Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic bacteroidetes. J. Biol. Chem. 2010; 285: 30261-73. doi: 10.1074/jbc.M110.141788 PMID: 20622018
35. Flint H. J., Scott K. P., Duncan S. H., Louis P. & Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012; 3 (4): 289-306. PMID: 22572875
36. Mariat D, Firmesse O, Levenez F, Guimaräes V, Sokol H, Doré J, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009; 9:123. doi: 10.1186/1471-2180-9-123 PMID: 19508720
37. Schwiertz A, Taras D, Schäfer K, Beijer S, Bos Na, Donus C, et al. Microbiota and SCFAin Lean and Overweight Healthy Subjects. Obesity 2010; 18: 190-195. doi: 10.1038/oby.2009.167 PMID: 19498350
38. Cinquin O. &Demongeot J. Positive and negative feedback: striking a balance between necessary antagonists. J. Theor. Biol. 2002; 216: 229-41. PMID: 12079373
39. Morohashi M, Winn AE, Borisuk MT, Bolouri H, Doyle J, Kitano H. Robustness as a measure of plausibility in models of biochemical networks. J. Theor. Biol. 2002; 216: 19-30. PMID: 12076125
40. Ananthasubramaniam B. & Herzel H. Positive Feedback Promotes Oscillations in Negative Feedback Loops. PLoS One 2014; 9: e104761. doi: 10.1371/journal.pone.0104761 PMID: 25126951
41. Bucci V., Nadell C. D. & Xavier J. B. The evolution of bacteriocin production in bacterial biofilms. Am. Nat. 2011; 178: E162-73. doi: 10.1086/662668 PMID: 22089878
42. Inglis R. F., Bayramoglu B., Gillor O. & Ackermann M. The role of bacteriocins as selfish genetic elements. Biol. Lett. 2013; 9 (3): 8-11.
43. Alcock J., Maley C. C. & Aktipis C. A. Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms. Bioessays 2014; 940-949. doi: 10.1002/bies.201400071 PMID: 25103109
44. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012; 150: 470-80. doi: 10.1016/j.cell.2012.07.008 PMID: 22863002
45. Carey H. V, Walters W. a & Knight R. Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013; 304: R33-42. doi: 10.1152/ajpregu.00387.2012 PMID: 23152108
46. Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, et al. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect. Immun. 2008; 76: 4726-36. doi: 10.1128/IAI.00319-08 PMID: 18678663
47. Shulzhenko N, Morgun A, Hsiao W, Battle M, Yao M, Gavrilova O, et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat. Med. 2011; 17: 1585-1593. doi: 10.1038/nm.2505 PMID: 22101768
48. Dethlefsen L. & Relman D. A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. PNAS 2011; 108: 4554-4561, doi: 10.1073/pnas.1000087107/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1000087 107 PMID: 20847294
49. Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 2012; 13: 440-7. doi: 10.1038/embor.2012.32 PMID: 22422004
50. Heinken A. & Thiele I. Systems biology of host-microbe metabolomics. Wiley Interdiscip. Rev. Syst. Biol. Med. 2015; 7: 195-219. doi: 10.1002/wsbm.1301 PMID: 25929487
51. Sahoo S., Haraldsdóttir H. S., Fleming R. M. T. & Thiele I. Modeling the effects of commonly used drugs on human metabolism. FEBS J. 2015; 282, 297-317. doi: 10.1111/febs.13128 PMID: 25345908
52. Theriot CM, Koenigsknecht MJ, PEC Jr, Hatton GE, Nelson AM, Li B, et al. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Natur. Com. 2014; 5:3114. doi: 10.1038/ncomms4114
53. Antonopoulos Da, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect. Immun. 2009; 77: 2367-75. doi: 10.1128/IAI.01520-08 PMID: 19307217
54. Tosh PK, McDonald LC. Infection Control in the Multidrug-Resistant Era: Tending the Human Microbiome. Clinical infectious diseases 2012; 54: 707-713. doi: 10.1093/cid/cir899 PMID: 22157322
55. Sommer M. O.A. & Dantas G. Antibiotics and the resistant microbiome. Curr. Opin. Microbiol. 2011; 14: 556-563. doi: 10.1016/j.mib.2011.07.005 PMID: 21802347
56. Vos M, DidelotXA comparison of homologous recombination rates in bacteria and archaea. ISME J. 2009; 3: 199-208. doi: 10.1038/ismej.2008.93 PMID: 18830278
57. Bucci V, Bradde S, Biroli G, Xavier JB. Social interaction, noise and antibiotic-mediated switches in the intestinal microbiota. PLoS Comput. Biol. 2012; 8: e1002497. doi: 10.1371/journal.pcbi.1002497 PMID: 22577356
58. Johnson S., Domínguez-García V., Donetti L. & Muñoz M. A. Trophic coherence determines food-web stability. Proc. Natl. Acad. Sci. U. S.A. 2014; 111: 17923-8. doi: 10.1073/pnas.1409077111 PMID: 25468963
59. Faust K, Raes J. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 2012; 10: 538-50. doi: 10.1038/nrmicro2832 PMID: 22796884
60. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, Lanz C et al. A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 2004; 303: 689-92. PMID: 14752164
61. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA. The application of ecological theory toward an understanding of the human microbiome. Science 2012; 336: 1255-62. doi: 10.1126/science.1224203 PMID: 22674335
62. Andersson DI, Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 2010; 8: 260-71. doi: 10.1038/nrmicro2319 PMID: 20208551
63. Tyakht A. V. et al. Human gut microbiota community structures in urban and rural populations in Russia. Nat. Commun. 4, 2469 (2013). doi: 10.1038/ncomms3469 PMID: 24036685
64. Hu Y, Yang X, Qin J, Lu N, Cheng G, Wu N et al. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat. Commun. 2013; 4: 2151. doi: 10.1038/ncomms3151 PMID: 23877117
65. Cerf-Bensussan N, Gaboriau-Routhiau V. The immune system and the gut microbiota: friends or foes? Nat. Rev. Immunol. 2010; 10: 735-44. doi: 10.1038/nri2850 PMID: 20865020
66. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009; 9: 313-23. doi: 10.1038/nri2515 PMID: 19343057
67. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 2010; 467: 426-9. doi: 10.1038/nature09415 PMID: 20864996
68. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR et al. Enterotypes of the human gut microbiome. Nature 2011; 473: 174-80. doi: 10.1038/nature09944 PMID: 21508958
69. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans AD, de Vos WM. Mucosa-Associated Bacteria in the Human Gastrointestinal Tract Are Uniformly Distributed along the Colon and Differfrom the Community Recovered from Feces. Appl. Environ. Microbiol. 2002; 68: 3401-3407. PMID: 12089021
70. Li X, LeBlanc J, Truong A, Vuthoori R, Chen SS, Lustgarten JL et al. A metaproteomic approach to study human-microbial ecosystems at the mucosal luminal interface. PLoS One 2011; 6: e26542. doi: 10.1371/journal.pone.0026542 PMID: 22132074
71. Panda S. Short-term effect of antibiotics on human gut microbiota. PLoS One 2014; 9: e95476. doi: 10.1371/journal.pone.0095476 PMID: 24748167
72. Wagener S, Shankar KR, Turnock RR, Lamont GL, Baillie CT. Colonic transit time - what is normal? J. Pediatr. Surg. 2004; 39:166-9; discussion 166-9. PMID: 14966733
73. Von Engelhardt W, Gros G, Burmester M, Hansen K, Becker G, Rechkemmer G. Functional role of bicarbonate in propionate transport across guinea-pig isolated caecum and proximal colon. J. Physiol. 1994; 477: Pt 2, 365-71. PMID: 7523661
74. Harig J. M., Soergel K. H., Barry J. A. & Ramaswamy K. Transport of propionate by human ileal brush-border membrane vesicles. Am. J. Physiol. 1991; 260: G776-82. PMID: 2035646
75. Bergman E. N. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 1990; 70: 567-90. PMID: 2181501
76. Den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 2013; 54: 2325-40. doi: 10.1194/jlr.R036012 PMID: 23821742