Clostridioides difficile 630Δerm in silico and in vivo – quantitative growth and extensive polysaccharide secretion

FEBS Open Bio

Volumn 7, Issue 4, 2017, Pages 602-615

  Dannheim, Henning ^a   Will, Sabine E ^a   Schomburg, Dietmar ^a   Neumann Schaal, Meina ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Clostridioides difficile; Clostridium difficile; exopolysaccharide; genome scale; metabolic modeling; metabolism

Indexed keywords

ACETYL COENZYME A; ALANINE; BACTERIAL POLYSACCHARIDE; GLUCOSE; GLUCOSE POLYMER; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACETYLATION; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL SECRETION SYSTEM; CITRIC ACID CYCLE; COMPUTER MODEL; COMPUTER SIMULATION; ENERGY METABOLISM; ENZYME SUBUNIT; GLUCONEOGENESIS; GLUCOSE TRANSPORT; GLYCOLYSIS; IN VIVO STUDY; LABORATORY TEST; MICROBIAL DEGRADATION; NONHUMAN; OPERON; OXIDATION REDUCTION REACTION; PEPTOCLOSTRIDIUM DIFFICILE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TIME;

EID: 85015405191     PISSN: 22115463     EISSN: None     Source Type: Journal    
DOI: 10.1002/2211-5463.12208     Document Type: Article

References (65)

1. Lawson PA, Citron DM, Tyrrell KL and Finegold SM (2016) Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O'Toole 1935) Prévot 1938. Anaerobe 40, 95–99.
2. Oren A and Garrity GM (2016) List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 66, 3761–3764.
3. Rupnik M, Wilcox MH and Gerding DN (2009) Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 7, 526–536.
4. Popoff MR, Rubin EJ, Gill DM and Boquet P (1988) Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain. Infect Immun 56, 2299–2306.
5. Eckert C, Emirian A, Le Monnier A, Cathala L, De Montclos H, Goret J, Berger P, Petit A, De Chevigny A, Jean-Pierre H et al. (2015) Prevalence and pathogenicity of binary toxin–positive Clostridium difficile strains that do not produce toxins A and B. New Microbes New Infect 3, 12–17.
6. Monot M, Eckert C, Lemire A, Hamiot A, Dubois T, Tessier C, Du-moulard B, Hamel B, Petit A, Lalande V et al. (2015) Clostridium difficile: new insights into the evolution of the pathogenicity locus. Sci Rep 5, 15023.
7. Karlsson S, Burman LG and Åkerlund T (1999) Suppression of toxin production in Clostridium difficile VPI 10463 by amino acids. Microbiology 145, 1683–1693.
8. Karlsson S, Lindberg A, Norin E, Burman LG and Åkerlund T (2000) Toxins, butyric acid, and other short-chain fatty acids are coordinately expressed and down-regulated by cysteine in Clostridium difficile. Infect Immun 68, 5881–5888.
9. Karlsson S, Burman LG and Åkerlund T (2008) Induction of toxins in Clostridium difficile is associated with dramatic changes of its metabolism. Microbiology 154, 3430–3436.
10. Neumann-Schaal M, Hofmann JD, Will SE and Schomburg D (2015) Time-resolved amino acid uptake of Clostridium difficile 630Δerm and concomitant fermentation product and toxin formation. BMC Microbiol 15, 281.
11. Stickland LH (1934) Studies in the metabolism of the strict anaerobes (genus Clostridium). Biochem J 28, 1746–1759.
12. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeño-Tárraga AM, Wang H et al. (2006) The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38, 779–786.
13. Hussain HA, Roberts AP and Mullany P (2005) Generation of an erythromycin-sensitive derivative of Clostridium difficile strain 630 (630Δerm) and demonstration that the conjugative transposon Tn916ΔE enters the genome of this strain at multiple sites. J Med Microbiol 54, 137–141.
14. van Eijk E, Anvar SY, Browne HP, Leung WY, Frank J, Schmitz AM, Roberts AP and Smits WK (2015) Complete genome sequence of the Clostridium difficile laboratory strain 630Δerm reveals differences from strain 630, including translocation of the mobile element CTn5. BMC Genom 16, 31.
15. Dannheim H, Riedel T, Neumann-Schaal M, Bunk B, Schober I, Spröer C, Chibani CM, Gronow S, Liesegang H, Overmann J et al. (2017) Manual curation and reannotation of the genomes of Clostridium difficile 630Δerm and Clostridium difficile 630. J Med Microbiol, doi: 10.1099/jmm.0.000427.
16. Durot M, Bourguignon PY and Schachter V (2009) Genome-scale models of bacterial metabolism: reconstruction and applications. FEMS Microbiol Rev 33, 164–190.
17. Varma A and Palsson BO (1994) Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110. Appl Environ Microbiol 60, 3724–3731.
18. Mahadevan R, Edwards JS and Doyle FJ III (2002) Dynamic flux balance analysis of diauxic growth in Escherichia coli. Biophys J 83, 1331–1340.
19. Larocque M, Chénard T and Najmanovich R (2014) A curated C. difficile strain 630 metabolic network: prediction of essential targets and inhibitors. BMC Syst Biol 8, 117.
20. McAnulty MJ, Yen JY, Freedman BG and Senger RS (2012) Genome-scale modeling using flux ratio constraints to enable metabolic engineering of clostridial metabolism in silico. BMC Syst Biol 6, 42.
21. Au J, Choi J, Jones SW, Venkataramanan KP and Antoniewicz MR (2014) Parallel labeling experiments validate Clostridium acetobutylicum metabolic network model for 13C metabolic flux analysis. Metab Eng 26, 23–33.
22. Amador-Noguez D, Feng XJ, Fan J, Roquet N, Rabitz H and Rabinowitz JD (2010) Systems-level metabolic flux profiling elucidates a complete, bifurcated tricarboxylic acid cycle in Clostridium acetobutylicum. J Bacteriol 192, 4452–4461.
23. Crown SB, Indurthi DC, Ahn WS, Choi J, Papoutsakis ET and Antoniewicz MR (2011) Resolving the TCA cycle and pentose-phosphate pathway of Clostridium acetobutylicum ATCC 824: isotopomer analysis, in vitro activities and expression analysis. Biotechnol J 6, 300–305.
24. Häggström L and Förberg C (1986) Significance of an extracellular polymer for the energy metabolism in Clostridium acetobutylicum: a hypothesis. Appl Microbiol Biotechnol 23, 234–239.
25. Lee SF, Forsberg CW and Gibbins LN (1985) Cellulolytic activity of Clostridium acetobutylicum. Appl Environ Microbiol 50, 220–228.
26. Sabathé F, Bélaïch A and Soucaille P (2002) Characterization of the cellulolytic complex (cellulosome) of Clostridium acetobutylicum. FEMS Microbiol Lett 217, 15–22.
27. Davies HA and Borriello SP (1990) Detection of capsule in strains of Clostridium difficile of varying virulence and toxigenicity. Microb Pathog 9, 141–146.
28. Ðapa T, Leuzzi R, Ng YK, Baban ST, Adamo R, Kuehne SA, Scarselli M, Minton NP, Serruto D and Unnikrishnan M (2013) Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. J Bacteriol 195, 545–555.
29. Monod J (1949) The growth of bacterial cultures. Annu Rev Microbiol 3, 371–394.
30. Hetzel M, Brock M, Selmer T, Pierik AJ, Golding BT and Buckel W (2003) Acryloyl-CoA reductase from Clostridium propionicum. Eur J Biochem 270, 902–910.
31. Buckel W and Thauer RK (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochim Biophys Acta 1827, 94–113.
32. Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W and Thauer RK (2008) Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J Bacteriol 190, 843–850.
33. Bertsch J, Parthasarathy A, Buckel W and Müller V (2013) An electron-bifurcating Caffeyl-CoA reductase. J Biol Chem 288, 11304–11311.
34. Weghoff MC, Bertsch J and Müller V (2014) A novel mode of lactate metabolism in strictly anaerobic bacteria. Environ Microbiol 17, 670–677.
35. Rühle T and Leister D (2015) Assembly of F1F0-ATP synthases. Biochim Biophys Acta 1847, 849–860.
36. Jiang W, Hermolin J and Fillingame RH (2001) The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. Proc Natl Acad Sci U S A 98, 4966–4971.
37. Toei M, Gerle C, Nakano M, Tani K, Gyobu N, Tamakoshi M, Sone N, Yoshida M, Fujiyoshi Y, Mitsuoka K et al. (2007) Dodecamer rotor ring defines H+/ATP ratio for ATP synthesis of prokaryotic V-ATPase from Thermus thermophilus. Proc Natl Acad Sci U S A 104, 20256–20261.
38. Stahlberg H, Müller DJ, Suda K, Fotiadis D, Engel A, Meier T, Matthey U and Dimroth P (2001) Bacterial Na+-ATP synthase has an undecameric rotor. EMBO Rep 2, 229–233.
39. Pogoryelov D, Yu J, Meier T, Vonck J, Dimroth P and Muller DJ (2005) The c15 ring of the Spirulina platensis F-ATP synthase: F1/F0 symmetry mismatch is not obligatory. EMBO Rep 6, 1040–1044.
40. Seelert H, Dencher NA and Müller DJ (2003) Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J Mol Biol 333, 337–344.
41. Meyer zu Tittingdorf JMW, Rexroth S, Schäfer E, Schlichting R, Giersch C, Dencher NA and Seelert H (2004) The stoichiometry of the chloroplast ATP synthase oligomer III in Chlamydomonas reinhardtii is not affected by the metabolic state. Biochim Biophys Acta 1659, 92–99.
42. Wolf J, Stark H, Fafenrot K, Albersmeier A, Pham TK, Müller KB, Meyer BH, Hoffmann L, Shen L, Albaum SP et al. (2016) A systems biology approach reveals major metabolic changes in the thermoacidic archaeon Sulfolobus soffataricus in response to the carbon source L-fucose versus D-glucose. Mol Microbiol 102, 882–908.
43. Lee NR, Lakshmanan M, Aggarwal S, Song JW, Karimi IA, Lee DY and Park JB (2014) Genome-scale metabolic network reconstruction and in silico flux analysis of the thermophilic bacterium Thermus thermophilus HB27. Microb Cell Fact 13, 61.
44. Trautwein K, Will SE, Hulsch R, Maschmann U, Wiegmann K, Hensler M, Michael V, Ruppersberg H, Wünsch D, Feenders C et al. (2016) Native plasmids restrict growth of Phaeobacter inhibens DSM 17395: energetic costs of plasmids assessed by quantitative physiological analyses. Environ Microbiol 12, 4817–4829.
45. Matyash V, Liebisch G, Kurzchalia TV, Shevchenko A and Schwudke D (2008) Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. J Lipid Res 49, 1137–1146.
46. Yang BY and Montgomery R (1996) Alkaline degradation of glucose: effect of initial concentration of reactants. Carbohydr Res 280, 27–45.
47. Cohen GH and Johnstone DB (1964) Extracellular polysaccharides of Azotobacter vinelandii. J Bacteriol 88, 329–338.
48. Lang M, Stelzer M and Schomburg D (2011) BKM-react, an integrated biochemical reaction database. BMC Biochem 12, 42.
49. Peltier J, Courtin P, Meouche IE, Lemée L, Chapot-Chartier MP and Pons JL (2011) Clostridium difficile has an original peptidoglycan structure with a high level of N-acetylglucosamine deacetylation and mainly 3-3 cross-links. J Biol Chem 286, 29053–29062.
50. Ganeshapillai J, Vinogradov E, Rousseau J, Weese JS and Monteiro MA (2008) Clostridium difficile cell-surface polysaccharides composed of pentaglycosyl and hexaglycosyl phosphate repeating units. Carbohydr Res 343, 703–710.
51. Poxton IR and Cartmill TDI (1982) Immunochemistry of the cell-surface carbohydrate antigens of Clostridium difficile. J Gen Microbiol 128, 1365–1370.
52. Neidhardt FC, Ingraham JL and Schaechter M (1990) Physiology of the bacterial cell: a molecular approach. Sinauer Associates, Sunderland, MA.
53. Machnicka MA, Milanowska K, Oglou OO, Purta E, Kurkowska M, Olchowik A, Januszewski W, Kalinowski S, Dunin-Horkawicz S, Rother KM et al. (2012) MODOMICS: a database of RNA modification pathways—2012 update. Nucleic Acids Res 41, gks1007.
54. Reid CW, Vinogradov E, Li J, Jarrell HC, Logan SM and Brisson JR (2012) Structural characterization of surface glycans from Clostridium difficile. Carbohydr Res 354, 65–73.
55. Dauner M and Sauer U (2001) Stoichiometric growth model for riboflavin-producing Bacillus subtilis. Biotechnol Bioeng 76, 132–143.
56. Drucker DB, Wardle HM and Boote V (1996) Phospholipid profiles of Clostridium difficile. J Bacteriol 178, 5844–5846.
57. Elsden SR, Hilton MG, Parsley KR and Self R (1980) The lipid fatty acids of proteolytic clostridia. J Gen Microbiol 118, 115–123.
58. Amador-Noguez D, Brasg IA, Feng XJ, Roquet N and Rabinowitz JD (2011) Metabolome remodeling during the acidogenic-solventogenic transition in Clostridium acetobutylicum. Appl Environ Microbiol 77, 7984–7997.
59. Thiele I and Palsson BO (2010) A protocol for generating a high-quality genome-scale metabolic reconstruction. Nat Protoc 5, 93–121.
60. Russell JB and Baldwin RL (1979) Comparison of maintenance energy expenditures and growth yields among several rumen bacteria grown on continuous culture. Appl Environ Microbiol 37, 537–543.
61. Orth JD, Thiele I and Palsson BO (2010) What is flux balance analysis? Nat Biotechnol 28, 245–248.
62. Riemer SA, Rex R and Schomburg D (2013) A metabolite-centric view on flux distributions in genome-scale metabolic models. BMC Syst Biol 7, 33.
63. Antoniewicz MR (2013) Dynamic metabolic flux analysis – tools for probing transient states of metabolic networks. Curr Opin Biotechnol 24, 973–978.
64. Lequeux G, Beauprez J, Maertens J, Van Horen E, Soetaert W, Van-damme E, Vanrolleghem PA, Lequeux G, Beauprez J, Maertens J et al. (2010) Dynamic metabolic flux analysis demonstrated on cultures where the limiting substrate is changed from carbon to nitrogen and vice versa. J Biomed Biotechnol 2010, e621645.
65. Kim J, Darley D and Buckel W (2005) 2-Hydroxyisocaproyl-CoA dehydratase and its activator from Clostridium difficile. FEBS J 272, 550–561.