Clostridium difficile colonizes alternative nutrient niches during infection across distinct murine gut microbiomes

mSystems

Volumn 2, Issue 4, 2017, Pages

  Jenior, Matthew L ^a   Leslie, Jhansi L ^a   Young, Vincent B ^a   Schloss, Patrick D ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Clostridium difficile; Infection; Metabolomics; Microbiome; Network modeling; Systems biology; Transcriptomics

Indexed keywords

EID: 85036640325     PISSN: None     EISSN: 23795077     Source Type: Journal    
DOI: 10.1128/mSystems.00063-17     Document Type: Article

References (59)

1. Lessa FC, Gould CV, McDonald LC. 2012. Current status of Clostridium difficile infection epidemiology. Clin Infect Dis 55(Suppl 2):S65-S70. https://doi.org/10.1093/cid/cis319.
2. Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, Farley MM, Holzbauer SM, Meek JI, Phipps EC, Wilson LE, Winston LG, Cohen JA, Limbago BM, Fridkin SK, Gerding DN, McDonald LC. 2015. Burden of Clostridium difficile infection in the United States. N Engl J Med 372: 825-834. https://doi.org/10.1056/NEJMoa1408913.
3. Leffler DA, Lamont JT. 2015. Clostridium difficile infection. N Engl J Med 372:1539-1548. https://doi.org/10.1056/NEJMra1403772.
4. Britton RA, Young VB. 2014. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 146: 1547-1553. https://doi.org/10.1053/j.gastro.2014.01.059.
5. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, Gerding DN, Kelly CP. 2008. A mouse model of Clostridium difficile-associated disease. Gastroenterology 135:1984-1992. https://doi.org/10.1053/j.gastro .2008.09.002.
6. Theriot CM, Koenigsknecht MJ, Carlson PE, Hatton GE, Nelson AM, Li B, Huffnagle GB, Li JZ, Young VB. 2014. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5:3114. https://doi.org/10 .1038/ncomms4114.
7. Schubert AM, Sinani H, Schloss PD. 2015. Antibiotic-induced alterations of the murine gut microbiota and subsequent effects on colonization resistance against Clostridium difficile. mBio 6:e00974-15. https://doi.org/ 10.1128/mBio.00974-15.
8. Antunes LCM, Han J, Ferreira RBR, Lolić P, Borchers CH, Finlay BB. 2011. Effect of antibiotic treatment on the intestinal metabolome. Antimicrob Agents Chemother 55:1494-1503. https://doi.org/10.1128/AAC .01664-10.
9. Ferreyra JA, Wu KJ, Hryckowian AJ, Bouley DM, Weimer BC, Sonnenburg JL. 2014. Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16:770-777. https://doi.org/10.1016/j.chom.2014.11.003.
10. Jump RLP, Polinkovsky A, Hurless K, Sitzlar B, Eckart K, Tomas M, Deshpande A, Nerandzic MM, Donskey CJ. 2014. Metabolomics analysis identifies intestinal microbiota-derived biomarkers of colonization resistance in clindamycin-treated mice. PLoS One 9:e101267. https://doi.org/10 .1371/journal.pone.0101267.
11. Freter R, Brickner H, Botney M, Cleven D, Aranki A. 1983. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun 39:676-685.
12. Wilson KH, Perini F. 1988. Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora. Infect Immun 56:2610-2614.
13. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeño-Tárraga AM, Wang H, Holden MTG, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38: 779-786. https://doi.org/10.1038/ng1830.
14. Kansau I, Barketi-Klai A, Monot M, Hoys S, Dupuy B, Janoir C, Collignon A. 2016. Deciphering adaptation strategies of the epidemic Clostridium difficile 027 strain during infection through in vivo transcriptional analysis. PLoS One 11:e0158204. https://doi.org/10.1371/journal .pone.0158204.
15. Songer JG, Anderson MA. 2006. Clostridium difficile: an important pathogen of food animals. Anaerobe 12:1-4. https://doi.org/10.1016/j.anaerobe.2005 .09.001.
16. Janvilisri T, Scaria J, Thompson AD, Nicholson A, Limbago BM, Arroyo LG, Songer JG, Gröhn YT, Chang YF. 2009. Microarray identification of Clostridium difficile core components and divergent regions associated with host origin. J Bacteriol 191:3881-3891. https://doi.org/10.1128/ JB.00222-09.
17. Gripp E, Hlahla D, Didelot X, Kops F, Maurischat S, Tedin K, Alter T, Ellerbroek L, Schreiber K, Schomburg D, Janssen T, Bartholomäus P, Hofreuter D, Woltemate S, Uhr M, Brenneke B, Grüning P, Gerlach G, Wieler L, Suerbaum S, Josenhans C. 2011. Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics 12:584. https://doi.org/10.1186/1471-2164-12-584.
18. Neumann-Schaal M, Hofmann JD, Will SE, Schomburg D. 2015. Timeresolved amino acid uptake of Clostridium difficile 630 Delta-erm and concomitant fermentation product and toxin formation. BMC Microbiol 15:281. https://doi.org/10.1186/s12866-015-0614-2.
19. Nawrocki KL, Edwards AN, Daou N, Bouillaut L, McBride SM. 2016. CodYdependent regulation of sporulation in Clostridium difficile. J Bacteriol 198:2113-2130. https://doi.org/10.1128/JB.00220-16.
20. Dineen SS, McBride SM, Sonenshein AL. 2010. Integration of metabolism and virulence by Clostridium difficile CodY. J Bacteriol 192:5350-5362. https://doi.org/10.1128/JB.00341-10.
21. Janoir C, Denève C, Bouttier S, Barbut F, Hoys S, Caleechum L, Chapetón-Montes D, Pereira FC, Henriques AO, Collignon A, Monot M, Dupuy B. 2013. Adaptive strategies and pathogenesis of Clostridium difficile from in vivo transcriptomics. Infect Immun 81:3757-3769. https://doi.org/10 .1128/IAI.00515-13.
22. Matamouros S, England P, Dupuy B. 2007. Clostridium difficile toxin expression is inhibited by the novel regulator TcdC. Mol Microbiol 64:1274-1288. https://doi.org/10.1111/j.1365-2958.2007.05739.x.
23. Antunes A, Martin-Verstraete I, Dupuy B. 2011. CcpA-mediated repression of Clostridium difficile toxin gene expression. Mol Microbiol 79: 882-899. https://doi.org/10.1111/j.1365-2958.2010.07495.x.
24. Theriot CM, Koumpouras CC, Carlson PE, Bergin II, Aronoff DM, Young VB. 2011. Cefoperazone-treated mice as an experimental platform to assess differential virulence of Clostridium difficile strains. Gut Microbes 2:326-334. https://doi.org/10.4161/gmic.19142.
25. Monot M, Boursaux-Eude C, Thibonnier M, Vallenet D, Moszer I, Medigue C, Martin-Verstraete I, Dupuy B. 2011. Reannotation of the genome sequence of Clostridium difficile strain 630. J Med Microbiol 60: 1193-1199. https://doi.org/10.1099/jmm.0.030452-0.
26. Koenigsknecht MJ, Theriot CM, Bergin IL, Schumacher CA, Schloss PD, Young VB. 2015. Dynamics and establishment of Clostridium difficile infection in the murine gastrointestinal tract. Infect Immun 83:934-941. https://doi.org/10.1128/IAI.02768-14.
27. Leslie JL, Huang S, Opp JS, Nagy MS, Kobayashi M, Young VB, Spence JR. 2015. Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect Immun 83:138-145. https://doi.org/10.1128/IAI .02561-14.
28. Antunes A, Camiade E, Monot M, Courtois E, Barbut F, Sernova NV, Rodionov DA, Martin-Verstraete I, Dupuy B. 2012. Global transcriptional control by glucose and carbon regulator CcpA in Clostridium difficile. Nucleic Acids Res 40:10701-10718. https://doi.org/10.1093/nar/gks864.
29. Bouillaut L, Dubois T, Sonenshein AL, Dupuy B. 2015. Integration of metabolism and virulence in Clostridium difficile. Res Microbiol 166: 375-383. https://doi.org/10.1016/j.resmic.2014.10.002.
30. Metcalf D, Sharif S, Weese JS. 2010. Evaluation of candidate reference genes in Clostridium difficile for gene expression normalization. Anaerobe 16:439-443. https://doi.org/10.1016/j.anaerobe.2010.06.007.
31. Gendron N, Putzer H, Grunberg-Manago M. 1994. Expression of both Bacillus subtilis threonyl-tRNA synthetase genes is autogenously regulated. J Bacteriol 176:486-494. https://doi.org/10.1128/jb.176.2.486-494 .1994.
32. Sjögren LL, Clarke AK. 2011. Assembly of the chloroplast ATP-dependent Clp protease in Arabidopsis is regulated by the ClpT accessory proteins. Plant Cell 23:322-332. https://doi.org/10.1105/tpc.110.082321.
33. Fimlaid KA, Bond JP, Schutz KC, Putnam EE, Leung JM, Lawley TD, Shen A. 2013. Global analysis of the sporulation pathway of Clostridium difficile. PLoS Genet 9:e1003660. https://doi.org/10.1371/journal.pgen .1003660.
34. Martin-Verstraete I, Peltier J, Dupuy B. 2016. The regulatory networks that control Clostridium difficile toxin synthesis. Toxins 8:E153. https:// doi.org/10.3390/toxins8050153.
35. Lee ASY, Song KP. 2005. LuxS/autoinducer-2 quorum sensing molecule regulates transcriptional virulence gene expression in Clostridium difficile. Biochem Biophys Res Commun 335:659-666. https://doi.org/10 .1016/j.bbrc.2005.07.131.
36. Jackson S, Calos M, Myers A, Self WT. 2006. Analysis of proline reduction in the nosocomial pathogen Clostridium difficile. J Bacteriol 188: 8487-8495. https://doi.org/10.1128/JB.01370-06.
37. Potapov AP, Voss N, Sasse N, Wingender E. 2005. Topology of mammalian transcription networks. Genome Inform 16:270-278.
38. Koschützki D, Schreiber F. 2008. Centrality analysis methods for biological networks and their application to gene regulatory networks. Gene Regul Syst Biol 2:193-201.
39. Ma HW, Zeng AP. 2003. The connectivity structure, giant strong component and centrality of metabolic networks. Bioinformatics 19:1423-1430. https:// doi.org/10.1093/bioinformatics/btg177.
40. Patil KR, Nielsen J. 2005. Uncovering transcriptional regulation of metabolism by using metabolic network topology. Proc Natl Acad Sci U S A 102:2685-2689. https://doi.org/10.1073/pnas.0406811102.
41. Karasawa T, Ikoma S, Yamakawa K, Nakamura S. 1995. A defined growth medium for Clostridium difficile. Microbiology 141:371-375. https://doi .org/10.1099/13500872-141-2-371.
42. Aboulnaga el-H, Pinkenburg O, Schiffels J, El-Refai A, Buckel W, Selmer T. 2013. Effect of an oxygen-tolerant bifurcating butyryl coenzyme A dehydrogenase/electron-transferring flavoprotein complex from Clostridium difficile on butyrate production in Escherichia coli. J Bacteriol 195:3704-3713. https://doi.org/10.1128/JB.00321-13.
43. Van Grinsven KW, Rosnowsky S, Van Weelden SW, Pütz S, Van Der Giezen M, Martin W, Van Hellemond JJ, Tielens AG, Henze K. 2008. Acetate: succinate CoA-transferase in the hydrogenosomes of Trichomonas vaginalis: identification and characterization. J Biol Chem 283: 1411-1418. https://doi.org/10.1074/jbc.M702528200.
44. Fuller MF, Reeds PJ. 1998. Nitrogen cycling in the gut. Annu Rev Nutr 18:385-411. https://doi.org/10.1146/annurev.nutr.18.1.385.
45. Marcobal A, Southwick AM, Earle KA, Sonnenburg JL. 2013. A refined palate: bacterial consumption of host glycans in the gut. Glycobiology 23:1038-1046. https://doi.org/10.1093/glycob/cwt040.
46. Rakoff-Nahoum S, Coyne MJ, Comstock LE. 2014. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol 24:40-49. https://doi.org/10.1016/j.cub.2013.10.077.
47. Green ML, Karp PD. 2006. The outcomes of pathway database computations depend on pathway ontology. Nucleic Acids Res 34:3687-3697. https://doi.org/10.1093/nar/gkl438.
48. Köpke M, Straub M, Dürre P. 2013. Clostridium difficile is an autotrophic bacterial pathogen. PLoS One 8:e62157. https://doi.org/10.1371/journal .pone.0062157.
49. Wilson KH, Kennedy MJ, Fekety FR. 1982. Use of sodium taurocholate to enhance spore recovery on a medium selective for Clostridium difficile. J Clin Microbiol 15:443-446.
50. Sorg JA, Sonenshein AL. 2010. Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid. J Bacteriol 192:4983-4990. https://doi.org/10.1128/JB.00610-10.
51. Kozich J, Westcott S, Baxter N, Highlander S, Schloss P. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112-5120. https://doi.org/10.1128/ AEM.01043-13.
52. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261-5267. https://doi.org/10.1128/AEM .00062-07.
53. Lopez-Medina E, Neubauer MM, Pier GB, Koh AY. 2011. RNA isolation of Pseudomonas aeruginosa colonizing the murine gastrointestinal tract. J Vis Exp. https://doi.org/10.3791/3293.
54. Martin MJ, Clare S, Goulding D, Faulds-Pain A, Barquist L, Browne HP, Pettit L, Dougan G, Lawley TD, Wren BW. 2013. The agr locus regulates virulence and colonization genes in Clostridium difficile 027. J Bacteriol 195:3672-3681. https://doi.org/10.1128/JB.00473-13.
55. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25.
56. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. 1999. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27:29-34. https://doi.org/10.1093/nar/27.1.29.
57. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079. https://doi.org/10.1093/bioinformatics/btp352.
58. Basler G, Ebenhöh O, Selbig J, Nikoloski Z. 2011. Mass-balanced randomization of metabolic networks. Bioinformatics 27:1397-1403. https://doi .org/10.1093/bioinformatics/btr145.
59. Bonett DG, Price RM. 2002. Statistical inference for a linear function of medians: confidence intervals, hypothesis testing, and sample size requirements. Psychol Methods 7:370-383. https://doi.org/10.1037/1082-989X.7.3.370.