The initial state of the human gut microbiome determines its reshaping by antibiotics

ISME Journal

Volumn 10, Issue 3, 2016, Pages 707-720

  Raymond, Frédéric ^a   Ouameur, Amin A ^a   Déraspe, Maxime ^a   Iqbal, Naeem ^a   Gingras, Hélène ^a   Dridi, Bédis ^a   Leprohon, Philippe ^a   Plante, Pier Luc ^a   Giroux, Richard ^a   Bérubé, Ève ^a   Frenette, Johanne ^a   Boudreau, Dominique K ^a   Simard, Jean Luc ^a   Chabot, Isabelle ^a   Domingo, Marc Christian ^b   Trottier, Sylvie ^a   Boissinot, Maurice ^a   Huletsky, Ann ^a   Roy, Paul H ^a   Ouellette, Marc ^a   Bergeron, Michel G ^a   Corbeil, Jacques ^a   more..

^a LAVAL UNIVERSITY   (Canada)

^b INSTITUT NATIONAL DE SANTÉ PUBLIQUE DU QUÉBEC   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIUM; DIGESTIVE SYSTEM; ENZYME ACTIVITY; GENE; GENE EXPRESSION; HOST-PATHOGEN INTERACTION; MICROBIAL COMMUNITY; OCCUPATIONAL EXPOSURE;

BACTEROIDES; ENTEROBACTER CLOACAE;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CEFPROZIL; CEPHALOSPORIN DERIVATIVE;

ADULT; BACTERIUM; CLASSIFICATION; DRUG EFFECTS; FECES; FEMALE; GENETICS; HUMAN; INTESTINE FLORA; ISOLATION AND PURIFICATION; MALE; METABOLISM; METAGENOMICS; MICROBIOLOGY; NORMAL HUMAN; YOUNG ADULT;

ADULT; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL PROTEINS; CEPHALOSPORINS; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HEALTHY VOLUNTEERS; HUMANS; MALE; METAGENOMICS; YOUNG ADULT;

EID: 84941243509     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.148     Document Type: Article

References (58)

1. Aagaard K, Petrosino J, Keitel W, Watson M, Katancik J, Garcia N, et al. (2013). The Human Microbiome Project strategy for comprehensive sampling of the human microbiome and why it matters. FASEB J. 27: 1012-1022.
2. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, MendeDR, et al. (2011). Enterotypes of the human gut microbiome. Nature. 473: 174-180.
3. Baysarowich J, Koteva K, Hughes DW, Ejim L, Griffiths E, Zhang K, et al. (2008). Rifamycin antibiotic resistance by ADP-ribosylation: structure and diversity of Arr. Proc Natl Acad Sci USA. 105: 4886-4891.
4. Beaber JW, Hochhut B, Waldor MK. (2004). SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature. 427: 72-74.
5. Benjamini Y, Yekutieli D. (2001). The control of the false discovery rate in multiple testing unDer DepenDency. Ann Stat. 29: 1165-1188.
6. Boisvert S, Laviolette F, Corbeil J. (2010). Ray: Simultaneous assembly of reads from a mix of high-Throughput sequencing technologies. J Comput Biol. 17: 1519-1533.
7. Boisvert S, Raymond F, Godzaridis E, Laviolette F, Corbeil J. (2012). Ray Meta: scalable Denovo metagenome assembly and profiling. Genome Biol. 13: R122.
8. Buffie CG, Jarchum I, Equinda M, Lipuma L, Gobourne A, Viale A, et al. (2012). Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect Immun. 80: 62-73.
9. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, et al. (2008). Decreased diversity of the fecal microbiome in recurrent Clostridium difficileassociated diarrhea. J Infect Dis. 197: 435-438.
10. Le Chatelier E, Nielsen T, Qin J, Prifti E, HilDebrand F, Falony G, et al. (2013). Richness of human gut microbiome correlates with metabolic markers. Nature. 500: 541-546.
11. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature. 505: 559-563.
12. Dethlefsen L, Huse S, Sogin ML, Relman DA. (2008). The pervasive effects of an antibiotic on the human gut microbiota, as revealed by Deep 16 S rRNA sequencing. PLoS Biol. 6: e280.
13. Dethlefsen L, Relman DA. (2011). Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci USA. 108: 4554-4561.
14. Dixon P. (2003). VEGAN, a package of R functions for community ecology. J Veg Sci. 14: 927-930.
15. Donia MS, Cimermancic P, Schulze CJ, Brown LCW, Martin J, Mitreva M, et al. (2014). A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell. 158: 1402-1414.
16. Dostal A, Chassard C, Hilty FM, Zimmermann MB, Jaeggi T, Rossi S, et al. (2012). Iron Depletion and repletion with ferrous sulfate or electrolytic iron modifies the composition and metabolic activity of the gut microbiota in rats. J Nutr. 142: 271-277.
17. Edlund C, Nord C. (2000). Effect on the human normal microflora of oral antibiotics for treatment of urinary tract infections. J Antimicrob Chemother. 46: 41-48.
18. Finegold SM, Molitoris D, Song Y, Liu C, Vaisanen M-L, Bolte E, et al. (2002). Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis. 35: S6-S16.
19. Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, et al. (2014). Bacterial phylogeny structures soil resistomes across habitats. Nature. 509: 612-616.
20. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G. (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science. 337: 1107-1111.
21. Forslund K, Sunagawa S, Coelho LP, Bork P. (2014). Metagenomic insights into the human gut resistome and the forces that shape it. Bioessays. 36: 316-329.
22. Forslund K, Sunagawa S, Kultima JR, MendeDR, Arumugam M, Typas A, et al. (2013). Country-specific antibiotic use practices impact the human gut resistome. Genome Res. 23: 1163-1169.
23. Franzosa EA, Huang K, Meadow JF, Gevers D, Lemon KP, Bohannan BJM, et al. (2015). IDentifying personal microbiomes using metagenomic coDes. Proc Natl Acad Sci. 112: E2930-E2938.
24. Ghosh TS, Gupta S, Sen, Nair GB, ManDeSS. (2013). In silico analysis of antibiotic resistance genes in the gut microflora of individuals from diverse geographies and age-groups. PLoS One. 8: e83823.
25. Haegeman B, Hamelin J, Moriarty J, Neal P, Dushoff J, Weitz JS. (2013). Robust estimation of microbial diversity in theory and in practice. ISME J. 7: 1092-1101.
26. HernánDez E, Bargiela R, Diez MS, Friedrichs A, Pérez-Cobas AE, Gosalbes MJ, et al. (2013). Functional consequences of microbial shifts in the human gastrointestinal tract linked to antibiotic treatment and obesity. Gut Microbes. 4: 306-315.
27. Hsiao EY, McBriDeSW, Hsien S, Sharon G, HyDeER, McCue T, et al. (2013). Microbiota modulate behavioral and physiological abnormalities associated with neuroDevelopmental disorDers. Cell. 155: 1451-1463.
28. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. (2010). Prodigal: prokaryotic gene recognition and translation initiation site iDentification. BMC Bioinformatics. 11: 119.
29. IzDebski R, Baraniak A, Herda M, Fiett J, Bonten MJM, Carmeli Y, et al. (2014). MLST reveals potentially highrisk international clones of Enterobacter cloacae. J Antimicrob Chemother. 70: 48-56.
30. Kampstra P. (2008). Beanplot : a boxplot alternative for visual comparison of distributions. J Stat Softw. 28: 1-9.
31. Kayser FH. (1994). In vitro activity of cefpodoxime in comparison with other oral beta-lactam antibiotics. Infection. 22: 370-375.
32. Li S, Josse J, Husson F. (2008). FactoMineR : An R package for multivariate analysis. J Stat Softw. 25: 1-18.
33. Legendre P, DeCáceres M. (2013). Beta diversity as the variance of community data: dissimilarity coefficients and partitioning. Ecol Lett. 16: 951-963.
34. Lewis SJ, Heaton KW. (1997). Stool form scale as a useful guiDeto intestinal transit time. Scand J Gastroenterol. 32: 920-924.
35. Li K, Bihan M, Yooseph S, Methé BA. (2012). Analyses of the microbial diversity across the human microbiome. PLoS One. 7: e32118.
36. Liu B, Pop M. (2009). ARDB-Antibiotic Resistance Genes Database. Nucleic Acids Res. 37: D443-D447.
37. LoDeH, Müller C, Borner K, Nord CE, Koeppe P. (1992). Multiple-dose pharmacokinetics of cefprozil and its impact on intestinal flora of volunteers. Antimicrob Agents Chemother. 36: 144-149.
38. Manges AR, Labbe A, Loo VG, Atherton JK, Behr MA, Masson L, et al. (2010). Comparative metagenomic study of alterations to the intestinal microbiota and risk of nosocomial Clostridum difficile-Associated disease. J Infect Dis. 202: 1877-1884.
39. Maurice CF, Haiser HJ, Turnbaugh PJ. (2013). Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell. 152: 39-50.
40. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, et al. (2013). The comprehensive antibiotic resistance database. Antimicrob Agents Chemother. 57: 3348-3357.
41. Pallav K, Dowd SE, Villafuerte J, Yang X, Kabbani T, Hansen J, et al. (2014). Effects of polysaccharopeptiDefrom Trametes versicolor and amoxicillin on the gut microbiome of healthy volunteers: a randomized clinical trial. Gut Microbes. 5: 458-467.
42. Pearson WR. (2000). Flexible sequence similarity searching with the FASTA3 program package. Methods Mol Biol. 132: 185-219.
43. Pérez-Cobas AE, Gosalbes MJ, Friedrichs A, Knecht H, Artacho A, Eismann K, et al. (2013). Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut. 62: 1591-1601.
44. Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys J-P. (2006). Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science. 313: 89-92.
45. Ren Z, Jiang J, Lu H, Chen X, He Y, Zhang H, et al. (2014). Intestinal microbial variation may predict early acute rejection after liver transplantation in rats. Transplantation. 98: 844-852.
46. Rodriguez-R LM, Konstantinidis KT. (2014). Estimating coverage in metagenomic data sets and why it matters. ISME J. 8: 2349-2351.
47. Song Y, Liu C, Finegold SM. (2004). Real-Time PCR quantitation of clostridia in feces of autistic children. Appl Environ Microbiol. 70: 6459-6465.
48. Song Y, Liu C, Molitoris DR, Tomzynski TJ, Lawson PA, Collins MD, et al. (2003). Clostridium bolteae sp nov, isolated from human sources. Syst Appl Microbiol. 26: 84-89.
49. Stecher B, Denzler R, Maier L, Bernet F, SanDers MJ, Pickard DJ, et al. (2012). Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc Natl Acad Sci USA. 109: 1269-1274.
50. Thorvaldsdóttir H, Robinson JT, Mesirov JP. (2013). Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 14: 178-192.
51. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. (2009). A core gut microbiome in obese and lean twins. Nature. 457: 480-484.
52. Ubeda C, Maiques E, Knecht E, Lasa I, Novick RP, PenaDés JR. (2005). Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity islanDencoDed virulence factors in staphylococci. Mol Microbiol. 56: 836-844.
53. Veleba M, DeMajumdar S, Hornsey M, Woodford N, SchneiDers T. (2013). Genetic characterization of tigecycline resistance in clinical isolates of Enterobacter cloacae and Enterobacter aerogenes. J Antimicrob Chemother. 68: 1011-1018.
54. Wang J, Stephan R, Power K, Yan Q, Hächler H, Fanning S. (2014). NucleotiDesequences of 705 16 transmissible plasmids iDentified in nine multidrugresistant Escherichia coli isolates expressing an ESBL phenotype isolated from food-producing animals and healthy humans. J Antimicrob Chemother. 69: 2658-2668.
55. WHO. (2014). Antimicrobial Resistance: Global Report on Surveillance 2014. World Health Organization: Geneva, Switzerland. http://www.who.int/mediacen tre/news/releases/2014/amr-report/en/.(accessed 3 July 2014
56. Wise R. (1994). Comparative microbiological activity and pharmacokinetics of cefprozil. Eur J Clin Microbiol Infect Dis. 13: 839-845.
57. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA, et al. (2011). Linking long-Term dietary patterns with gut microbial enterotypes. Science. 334: 105-108.
58. Yutin N, Galperin MY. (2013). A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol. 15: 2631-2641.