A link between gut community metabolism and pathogenesis: Molecular hydrogen-stimulated glucarate catabolism aids Salmonella virulence

Open Biology

Volumn 3, Issue 1 DEC, 2013, Pages

  Lamichhane Khadka, Reena ^a,b   Benoit, Stephane L ^a   Maier, Susan E ^a   Maier, Robert J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b SAINT MARY'S COLLEGE   (United States)

Author keywords

Carbon transport; Gut microbiome; In vivo pathogen growth; Metabolism and virulence; Microbial carbon utilization

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; GLUTARIC ACID DERIVATIVE; HYDROGEN; VIRULENCE FACTOR;

ANIMAL; ANIMAL SALMONELLOSIS; ARTICLE; BAGG ALBINO MOUSE; CARBON TRANSPORT; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; GUT MICROBIOME; IN VIVO PATHOGEN GROWTH; LIVER; METABOLISM; METABOLISM AND VIRULENCE; MICROBIAL CARBON UTILIZATION; MICROBIOLOGY; MOUSE; MUTATION; PATHOGENICITY; PATHOLOGY; SALMONELLA TYPHIMURIUM; SPLEEN;

CARBON TRANSPORT; GUT MICROBIOME; IN VIVO PATHOGEN GROWTH; METABOLISM AND VIRULENCE; MICROBIAL CARBON UTILIZATION;

ANIMALS; BACTERIAL PROTEINS; FEMALE; GLUTARATES; HYDROGEN; LIVER; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED BALB C; MUTATION; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SPLEEN; VIRULENCE FACTORS;

EID: 84897500886     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.130146     Document Type: Article

References (40)

1. Anet EFJ, Reynolds TM. 1954 Isolation of mucic acid from fruits. Nature 174, 930-932. (doi:10.1038/ 174930a0)
2. Whiting GC, Coggins RA. 1960 Organic acid metabolism in cider and perry fermentations. III. Keto-acids in cider-apple juices and ciders. J. Sci. Food. Agric. 11, 337-341. (doi:10.1002/jsfa. 2740110608)
3. Marsh CA. 1985 An enzymatic determination of D-glucaric acid by conversion to pyruvate. Anal. Biochem. 145, 266-272. (doi:10.1016/0003- 2697(85)90360-4) (Pubitemid 15100955)
4. Matsui M, Fukuo A, Watanabe Y, Wanibe T, Okada M. 1977 Studies on the glucaric acid pathway in the metabolism of D-glucuronic acid in mammals. IV. Fluorometric method for the determination of glucaric acid in serum. Chem. Pharm. Bull. 20, 845-848. (doi:10.1248/cpb.20.845)
5. Dutton GJ. 1980 Glucuronidation of drugs and other compounds, pp. 83-89. Boca Raton, FL: CRC Press
6. Moon TS, Yoon S, Lanza AM, Rot-Mayhew JD, Jones-Prather KL. 2009 Production of glucaric acid from a synthetic pathway in recombinant Escherichia coli. Appl. Environ. Microbiol. 75, 589-595. (doi:10.1128/AEM.00973-08)
7. Webb TE, Abou-Issa H, Stromberg PC, Curley Jr RC, Nguyen MH. 1993 Mechanism of growth inhibition of mammary carcinomas by glucarate and the glucarate: retinoid combination. Anticancer Res. 13, 2095-2099 (Pubitemid 24036332)
8. Lajolo C, Sgambato A, Maiorano E, Lucchese A, Favia E, Giuliani M. 2010 Calcium glucarate inhibits DMBA-induced oral carcinogenesis in the hamster: histomorphometric evaluation. Anticancer Res. 30, 843-849
9. Blumenthal HJ, Lucuta VL, Blumenthal DC. 1990 Specific enzymatic assay for D-glucarate in human serum. Anal. Biochem. 185, 286-293. (doi:10. 1016/0003-2697(90)90294-J) (Pubitemid 20107163)
10. Hunter J, Maxwell J, Carrella M, Stewart DA, Williams R. 1971 Urinary D-glucaric acid excretion as a measure of hepatic enzyme induction in man. Clinic. Sci. 17, 564-571. (doi:10.1042/cs040010P)
11. Foster JW, Spector MP. 1995 How Salmonella survive against the odds. Annu. Rev. Microbiol. 49, 145-174. (doi:10.1146/annurev.micro.49.1.145)
12. Kwon YM, Ricke SC. 1998 Survival of a Salmonella typhimurium poultry isolate in the presence of propionic acid under aerobic and anaerobic conditions. Anaerobe 4, 251-256. (doi:10.1006/ anae.1998.0177) (Pubitemid 29353670)
13. Becker D, Selbach C, Rollenhagen MC, Ballmaier M, Meyer TF, Mann M, Bumann D. 2006 Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440, 303-307. (doi:10.1038/ nature04616)
14. Bumann D. 2009 System-level analysis of Salmonella metabolism during infection. Curr. Opin. Microbiol. 12, 559-567. (doi:10.1016/j. mib2009.08.004)
15. Trudgill PW, Widdus R. 1966 D-glucarate catabolism by pseudomonadaceae and enterobacteriaceae. Nature 211, 1097-1099. (doi:10.1038/2111097a0)
16. Sharma BS, Blumenthal HJ. 1973 Catabolism of D-glucaric acid to a-ketoglutarate in Bacillus megaterium. J. Bacteriol. 116, 1346-1354
17. Roberton AM, Sullivan PA, Jones-Mortimer MC, Kornberg HL. 1980 Two genes affecting glucarate utilization in Escherichia coli K12. J. Gen. Microbiol. 117, 311-382. (doi:10.1099/0022187- 117-2-377)
18. Ansong C et al. 2013 Top-down proteomics reveals a unique protein S-thiolation switch in Salmonella Typimurium in response to infection-like conditions. Proc. Natl Acad. Sci. USA 110, 10 153-10 158. (doi:10.1073/pnas. 1221210110)
19. Maier RJ. 2005 Use of molecular hydrogen as an energy substrate by human pathogenic bacteria. Biochem. Soc. Trans. 33, 83-85. (doi:10.1042/ BST0330083) (Pubitemid 40313767)
20. Maier RJ, Olczak A, Maier S, Soni S, Gunn J. 2004 Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect. Immun. 72, 6294-6299. (doi:10.1128/ IAI.72.11.6294-6299.2004) (Pubitemid 39425407)
21. Lamichhane-Khadka R, Kwiatkowski A, Maier RJ. 2010 The Hyb Hydrogenase permits hydrogendependent respiratory growth of Salmonella enterica serovar Typhimurium. mBio 1, e00284. (doi:10. 1128/mBio.00284-10)
22. Mehta NS, Benoit S, Mysore JV, Sousa RS, Maier RJ. 2005 Helicobacter hepaticus hydrogenase mutants are deficient in hydrogen-supported amino acid uptake and in causing liver lesions in A/J mice. Infect. Immun. 73, 5311-5318. (doi:10.1128/ AI.73.9.5311-5318.2005) (Pubitemid 41192964)
23. Lamichhane-Khadka R, Frye JG, Porwollik S, McClelland M, Maier RJ. 2011 Hydrogen-stimulated carbon acquisition and conservation in Salmonella enterica serovar Typhimurium. J. Bacteriol. 193, 5824-5832. (doi:10.1128/JB.05456-11)
24. Hubbard BK, Koch M, Palmer DR, Babbitt PC, Gerit JA. 1998 Evolution of the enzymatic activities in the enolase superfamily: characterization of the (D)- glucarate/galactarate catabolic pathway in Escherichia coli. Biochemistry 37, 14 369-14 375. (doi:10.1021/bi981124F) (Pubitemid 28489042)
25. Schmidt DMZ, Hubbard BK, Gerlt JA. 2001 Evolution of enzymatic activities in the enolase superfamily: identification of the general acid catalyst in the active site of D-glucarate dehydratase from Escherichia coli. Biochemistry 40, 10 054-10 062. (doi:10.1021/bi011640x) (Pubitemid 34015199)
26. Yew WS, Fedorov AA, Fedorov EV, Almo SC, Gerlt JA. 2007 Evolution of the enzymatic activities in the enolase superfamily: L-talarate/Galactarate dehydratase from Salmonella typhimurium LT2. Biochemistry 46, 9564-9577. (doi.10.1021/ bi7008882) (Pubitemid 47291963)
27. Aghaie A et al. 2008 New Insights into the alternative D-glucarate degradation pathway. J. Biol. Chem. 283, 15 638-15 646. (doi:10.1074/jbc. M800487200)
28. Zbell AL, Maier RJ. 2009 Role of the Hya hydrogenase in recycling of anaerobically produced H2 in Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 75, 1456-1459. (doi:10.1128/AEM.02064.08)
29. Sawers RG, Jamieson DJ, Higgins CF, Boxer DH. 1986 Characterization and physiological roles of membrane-bound hydrogenase isoenzymes from Salmonella typhimurium. J. Bacteriol. 168, 398-404 (Pubitemid 16001628)
30. Gutnick D, Calvo JM, Klopotowski T, Ames BN. 1969 Compounds which serve as the sole source of carbon or nitrogen for Salmonella Typhimurium LT-2. J. Bacteriol. 100, 215-219
31. Gotz A, Goebel W. 2010 Glucose and glucose 6-phosphate as carbon sources in extra- and intracellular growth of enteroinvasive Esherichia coli and Salmonella enterica. Microbiology 156, 1176-1187. (doi:10.1099/mic.0.034744-0)
32. Chaudhuri RR et al. 2013 Comprehensive assignment of roles for Salmonella Typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet. 9, e1003456. (doi:10.1371/ journal.pgen.1003456)
33. Bowden SD, Rowley G, Hinton JCD, Thompson A. 2009 Glucose and glycolysis are required for the successful infection of macrophages and mice by Salmonella enterica serovar Typhimurium. Infect. Immun. 77, 3117-3126. (doi:10.11128/ AI.00093-09)
34. Götz A, Eylert E, Eisenreich W, Goebel W. 2010 Carbon metabolism of enterobacterial human pathogens growing in epithelial colorectal adenocarcinoma (Caco-2) cells. PLoS ONE 5, e10586. (doi:10.1371/journal.pone.0010586)
35. Eisenreich W, Dandekar T, Heesemann J, Goebel W. 2010 Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat. Rev. Microbiol. 8, 401-412. (doi:10.1038/nrmicro2351)
36. AbuOun M, Suthers PF, Jones GI, Carter BR, Saunders MP, Maranas CD, Woodward MJ, Anjum MF. 2009 Genome scale reconstruction of a Salmonella metabolic model: comparison of similarity and differences with a commensal Escherichia coli strain. J. Biol. Chem. 284, 29 480- 29 488. (doi:10.1074/jbc.M109.005868)
37. Datsenko KA, Wanner BL. 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640-6645. (doi:10.1073/pnas. 120163297) (Pubitemid 30412767)
38. Warren JW, Walker JR, Roth JR, Altman E. 2000 Construction and characterization of a highly regulable expression vector, pLAC11, and its multipurpose derivatives, pLAC22 and pLAC33. Plasmid 44, 138-151. (doi:10.1006/plas.2000.1477)
39. Sambrook J, Fritsch EF, Maniatis T. 1989 Molecular cloning, a laboratory manual, 2nd edn, vol. III: A.3. Cold Spring Harbor Laboratory Press: New York
40. Tamayo R, Ryan SS, McCoy AJ, Gunn JS. 2002 Identification and genetic characterization of PmrAregulated genes and genes involved in polymyxin B resistance in Salmonella enterica serovar typhimurium. Infect. Immun. 70, 6770-6778. (doi:10.1128/IAI.70.12.6770-6778.2002) (Pubitemid 35387908)