Metabolomics analysis identifies intestinal microbiota-derived biomarkers of colonization resistance in clindamycin-treated mice

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Jump, Robin L P ^a,b   Polinkovsky, Alex ^c   Hurless, Kelly ^c   Sitzlar, Brett ^c   Eckart, Kevin ^c   Tomas, Myreen ^b   Deshpande, Abhishek ^c   Nerandzic, Michelle M ^c   Donskey, Curtis J ^a,b,c  

^a GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CLINDAMYCIN; PIPERACILLIN PLUS TAZOBACTAM; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL SPORE; CLOSTRIDIUM DIFFICILE; COLONIZATION RESISTANCE; CONTROLLED STUDY; ENTEROCOCCUS; FECES ANALYSIS; FEMALE; IN VIVO STUDY; INTESTINE FLORA; LACHNOSPIRACEAE; METABOLOMICS; MOUSE; NONHUMAN; PROTEIN METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; RUMINOCOCCACEAE; ANIMAL; BACTERIA; DRUG EFFECTS; INTESTINE; METABOLISM; METABOLOME; MICROBIOLOGY; MICROFLORA; PROCEDURES;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BIOLOGICAL MARKERS; CLINDAMYCIN; FEMALE; INTESTINES; METABOLOME; METABOLOMICS; MICE; MICROBIOTA;

EID: 84903785994     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101267     Document Type: Article

References (50)

1. Blaut M, Clavel T (2007) Metabolic Diversity of the Intestinal Microbiota: Implications for Health and Disease. J Nutr 137: 751S-755S. (Pubitemid 46397515)
2. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307: 1915-1920. doi:10.1126/science.1104816. (Pubitemid 40404694)
3. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, et al. (2005) Diversity of the Human Intestinal Microbial Flora. Science 308: 1635-1638. doi:10.1126/science.1110591. (Pubitemid 40807514)
4. Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK (2011) Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol 19: 349-359. doi:10.1016/j.tim.2011.05.006.
5. Lawley TD, Walker AW (2013) Intestinal colonization resistance. Immunology 138: 1-11. doi:10.1111/j.1365-2567.2012.03616.x.
6. Van der Waaij D, Vries JMB, der Wees JECL (1971) Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond) 69: 405-411.
7. Stiefel U, Pultz NJ, Marion S. Helfand M, Donskey CJ (2004) Increased Susceptibility to Vancomycin-Resistant Enterococcus Intestinal Colonization Persists After Completion of Anti-Anaerobic Antibiotic Treatment In Mice. Infect Control Hosp Epidemiol 25: 373-379. (Pubitemid 38621082)
8. Pultz NJ, Donskey CJ (2005) Effect of Antibiotic Treatment on Growth of and Toxin Production by Clostridium difficile in the Cecal Contents of Mice. Antimicrob Agents Chemother 49: 3529-3532. doi:10.1128/AAC.49.8.3529- 3532.2005.
9. Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB (2012) Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect Immun 80: 3786-3794. doi:10.1128/IAI.00647-12.
10. Buffie CG, Jarchum I, Equinda M, Lipuma L, Gobourne 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. doi:10.1128/IAI.05496-11.
11. Lawley TD, Clare S, Walker AW, Stares MD, Connor TR, et al. (2012) Targeted Restoration of the Intestinal Microbiota with a Simple, Defined Bacteriotherapy Resolves Relapsing Clostridium difficile Disease in Mice. PLoS Pathog 8: e1002995. doi:10.1371/journal.ppat.1002995.
12. Rolfe RD (1984) Role of volatile fatty acids in colonization resistance to Clostridium difficile. Infect Immun 45: 185-191.
13. Nerandzic MM, Donskey CJ (2009) Effective and Reduced-Cost Modified Selective Medium for Isolation of Clostridium difficile. J Clin Microbiol 47: 397-400. doi:10.1128/JCM.01591-08.
14. Rolfe RD, Finegold SM (1983) Intestinal b-Lactamase Activity in Ampicillin-Induced, Clostridium difficile-Associated Ileocecitis. J Infect Dis 147: 227-235. doi:10.1093/infdis/147.2.227. (Pubitemid 13195101)
15. Louie TJ, Cannon K, Byrne B, Emery J, Ward L, et al. (2012) Fidaxomicin Preserves the Intestinal Microbiome During and After Treatment of Clostridium difficile Infection (CDI) and Reduces Both Toxin Reexpression and Recurrence of CDI. Clin Infect Dis 55: S132-S142. doi:10.1093/cid/cis338.
16. Rinttilä T, Kassinen A, Malinen E, Krogius L, Palva A (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97: 1166-1177. doi:10.1111/j.1365-2672.2004.02409.x. (Pubitemid 39573940)
17. Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148: 257-266. (Pubitemid 34083204)
18. Bernhard AE, Field KG (2000) A PCR Assay To Discriminate Human and Ruminant Feces on the Basis of Host Differences in Bacteroides-Prevotella Genes Encoding 16S rRNA. Appl Environ Microbiol 66: 4571-4574. doi:10.1128/AEM.66.10. 4571-4574.2000.
19. Bartosch S, Fite A, Macfarlane GT, McMurdo MET (2004) Characterization of Bacterial Communities in Feces from Healthy Elderly Volunteers and Hospitalized Elderly Patients by Using Real-Time PCR and Effects of Antibiotic Treatment on the Fecal Microbiota. Appl Environ Microbiol 70: 3575-3581. doi:10.1128/AEM.70. 6.3575-3581.2004. (Pubitemid 38745906)
20. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, et al. (2002) Development of 16S rRNA-Gene-Targeted Group-Specific Primers for the Detection and Identification of Predominant Bacteria in Human Feces. Appl Environ Microbiol 68: 5445-5451. doi:10.1128/AEM.68.11.5445-5451.2002. (Pubitemid 35265679)
21. Delroisse J-M, Boulvin A-L, Parmentier I, Dauphin RD, Vandenbol M, et al. (2008) Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Microbiol Res 163: 663-670.
22. Loy A, Horn M, Wagner M (2003) probeBase: an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res 31: 514-516. (Pubitemid 36157288)
23. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-596. doi:10.1093/nar/gks1219.
24. R Development Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available: URL http://www.R-project.org/.
25. Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E (2009) Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem 81: 6656-6667. doi:10.1021/ac901536h.
26. Dehaven CD, Evans AM, Dai H, Lawton KA (2010) Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J Cheminformatics 2: 9. doi:10.1186/1758-2946-2-9.
27. M. Evans A (2012) Categorizing Ion -Features in Liquid Chromatography/Mass Spectrometry Metobolomics Data. J Postgenomics Drug Biomark Dev 02. Available: http://www.omicsonline.org/2153-0769/2153-0769-2-110.php?aid= 5372. Accessed 23 June 2013.
28. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445. doi:10.1073/pnas.1530509100. (Pubitemid 37033947)
29. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38: D355-360. doi:10.1093/nar/gkp896.
30. Wishart DS, Jewison T, Guo AC, Wilson M, Knox C, et al. (2013) HMDB 3.0 - The Human Metabolome Database in 2013. Nucleic Acids Res 41: D801-807. doi:10.1093/nar/gks1065.
31. Wyss M, Kaddurah-Daouk R (2000) Creatine and Creatinine Metabolism. Physiol Rev 80: 1107-1213. (Pubitemid 30452013)
32. Rowland IR, Wiseman H, Sanders TAB, Adlercreutz H, Bowey EA (2000) Interindividual Variation in Metabolism of Soy Isoflavones and Lignans: Influence of Habitual Diet on Equol Production by the Gut Microflora. Nutr Cancer 36: 27-32. doi:10.1207/S15327914NC3601-5. (Pubitemid 30317832)
33. Macfarlane GT, Macfarlane S (2012) Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int 95: 50-60.
34. SEGAL S, FOLEY J (1958) The metabolism of D-ribose in man. J Clin Invest 37: 719-735. doi:10.1172/JCI103658.
35. Tronick SR, Ciardi JE, Stadtman ER (1973) Comparative Biochemical and Immunological Studies of Bacterial Glutamine Synthetases. J Bacteriol 115: 858-868.
36. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, et al. (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci 106: 3698-3703. doi:10.1073/pnas.0812874106.
37. Chung KT, Anderson GM, Fulk GE (1975) Formation of indoleacetic acid by intestinal anaerobes. J Bacteriol 124: 573-575.
38. Vincent C, Stephens DA, Loo VG, Edens TJ, Behr MA, et al. (2013) Reductions in intestinal Clostridiales precede the development of nosocomial Clostridium difficile infection. Microbiome 1: 18. doi:10.1186/2049-2618-1-18.
39. Antharam VC, Li EC, Ishmael A, Sharma A, Mai V, et al. (2013) Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbiol 51: 2884-2892. doi:10.1128/JCM.00845-13.
40. Welling GW, Groen G, Tuinte JH, Koopman JP, Kennis HM (1980) Biochemical effects on germ-free mice of association with several strains of anaerobic bacteria. J Gen Microbiol 117: 57-63. (Pubitemid 10099612)
41. Yap IKS, Li JV, Saric J, Martin F-P, Davies H, et al. (2008) Metabonomic and microbiological analysis of the dynamic effect of vancomycin-induced gut microbiota modification in the mouse. J Proteome Res 7: 3718-3728. doi:10.1021/pr700864x.
42. Romick-Rosendale LE, Goodpaster AM, Hanwright PJ, Patel NB, Wheeler ET, et al. (2009) NMR-based metabonomics analysis of mouse urine and fecal extracts following oral treatment with the broad-spectrum antibiotic enrofloxacin (Baytril). Magn Reson Chem MRC 47 Suppl 1: S36-46. doi:10.1002/mrc.2511.
43. Swann JR, Tuohy KM, Lindfors P, Brown DT, Gibson GR, et al. (2011) Variation in antibiotic-induced microbial recolonization impacts on the host metabolic phenotypes of rats. J Proteome Res 10: 3590-3603. doi:10.1021/ pr200243t.
44. Theriot CM, Koenigsknecht MJ, Carlson Jr PE, Hatton GE, Nelson AM, et al. (2014) Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5. Available: http://www.nature.com/ncomms/2014/140120/ncomms4114/full/ncomms4114. html. Accessed 6 May 2014.
45. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, et al. (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502. Available: http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC3825626/. Accessed 6 May 2014.
46. Abujamel T, Cadnum JL, Jury LA, Sunkesula VCK, Kundrapu S, et al. (2013) Defining the Vulnerable Period for Re-Establishment of Clostridium difficile Colonization after Treatment of C. difficile Infection with Oral Vancomycin or Metronidazole. PloS One 8: e76269. doi:10.1371/journal.pone.0076269.
47. Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, et al. (2011) The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile Infection. Gut Microbes 2: 145-158.
48. Jump RLP, Pultz MJ, Donskey CJ (2007) Vegetative Clostridium difficile Survives in Room Air on Moist Surfaces and in Gastric Contents with Reduced Acidity: a Potential Mechanism To Explain the Association between Proton Pump Inhibitors and C. difficile-Associated Diarrhea? Antimicrob Agents Chemother 51: 2883-2887. doi:10.1128/AAC.01443-06.
49. Donskey CJ, Chowdhry TK, Hecker MT, Hoyen CK, Hanrahan JA, et al. (2000) Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients. N Engl J Med 343: 1925-1932. doi:10.1056/NEJM200012283432604. (Pubitemid 32064786)
50. Lerner A, Romano J, Chmelnitsky I, Navon-Venezia S, Edgar R, et al. (2013) Rectal swabs are suitable for quantifying the carriage load of KPC-producing carbapenem-resistant Enterobacteriaceae. Antimicrob Agents Chemother 57: 1474-1479. doi:10.1128/AAC.01275-12.