1887

Abstract

Carnitine is a quaternary amine compound found at high concentration in animal tissues, particularly muscle, and is most well studied for its contribution to fatty acid transport into mitochondria. In bacteria, carnitine is an important osmoprotectant, and can also enhance thermotolerance, cryotolerance and barotolerance. Carnitine can be transported into the cell or acquired from metabolic precursors, where it can serve directly as a compatible solute for stress protection or be metabolized through one of a few distinct pathways as a nutrient source. In this review, we summarize what is known about carnitine physiology and metabolism in bacteria. In particular, recent advances in the aerobic and anaerobic metabolic pathways as well as the use of carnitine as an electron acceptor have addressed some long-standing questions in the field.

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2015-06-01
2019-12-16
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References

  1. Achouak W. , Christen R. , Barakat M. , Martel M. H. , Heulin T. . ( 1999;). Burkholderia caribensis sp. nov., an exopolysaccharide-producing bacterium isolated from vertisol microaggregates in Martinique. . Int J Syst Bacteriol 49:, 787–794 [CrossRef] [PubMed].
    [Google Scholar]
  2. Angelidis A. S. , Smith G. M. . ( 2003;). Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium. . Appl Environ Microbiol 69:, 7492–7498 [CrossRef] [PubMed].
    [Google Scholar]
  3. Angelidis A. S. , Smith L. T. , Hoffman L. M. , Smith G. M. . ( 2002;). Identification of opuC as a chill-activated and osmotically activated carnitine transporter in Listeria monocytogenes . . Appl Environ Microbiol 68:, 2644–2650 [CrossRef] [PubMed].
    [Google Scholar]
  4. Aragozzini F. , Manzoni M. , Cavazzoni V. , Craveri R. . ( 1986;). d,l-Carnitine resolution by Fusarium oxysporum . . Biotechnol Lett 8:, 95–97 [CrossRef].
    [Google Scholar]
  5. Arima J. , Uesumi A. , Mitsuzumi H. , Mori N. . ( 2010;). Biochemical characterization of l-carnitine dehydrogenases from Rhizobium sp. and Xanthomonas translucens . . Biosci Biotechnol Biochem 74:, 1237–1242 [CrossRef] [PubMed].
    [Google Scholar]
  6. Aurich H. , Kleber H. P. , Schöpp W. D. . ( 1967;). An inducible carnitine dehydrogenase from Pseudomonas aeruginosa . . Biochim Biophys Acta 139:, 505–507. [CrossRef] [PubMed]
    [Google Scholar]
  7. Barbier M. , Owings J. P. , Martínez-Ramos I. , Damron F. H. , Gomila R. , Blázquez J. , Goldberg J. B. , Albertí S. . ( 2013;). Lysine trimethylation of EF-Tu mimics platelet-activating factor to initiate Pseudomonas aeruginosa pneumonia. . MBio 4:, e00207–e00213. [CrossRef] [PubMed]
    [Google Scholar]
  8. Barrett E. L. , Kwan H. S. . ( 1985;). Bacterial reduction of trimethylamine oxide. . Annu Rev Microbiol 39:, 131–149. [CrossRef] [PubMed]
    [Google Scholar]
  9. Bastard K. , Smith A. A. , Vergne-Vaxelaire C. , Perret A. , Zaparucha A. , De Melo-Minardi R. , Mariage A. , Boutard M. , Debard A. , other authors . ( 2014;). Revealing the hidden functional diversity of an enzyme family. . Nat Chem Biol 10:, 42–49. [CrossRef] [PubMed]
    [Google Scholar]
  10. Bayles D. O. , Wilkinson B. J. . ( 2000;). Osmoprotectants and cryoprotectants for Listeria monocytogenes . . Lett Appl Microbiol 30:, 23–27. [CrossRef] [PubMed]
    [Google Scholar]
  11. Begley M. , Gahan C. G. , Hill C. . ( 2005;). The interaction between bacteria and bile. . FEMS Microbiol Rev 29:, 625–651. [CrossRef] [PubMed]
    [Google Scholar]
  12. Bennett B. J. , de Aguiar Vallim T. Q. , Wang Z. , Shih D. M. , Meng Y. , Gregory J. , Allayee H. , Lee R. , Graham M. , other authors . ( 2013;). Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. . Cell Metab 17:, 49–60. [CrossRef] [PubMed]
    [Google Scholar]
  13. Bernal V. , Arense P. , Blatz V. , Mandrand-Berthelot M. A. , Cánovas M. , Iborra J. L. . ( 2008;). Role of betaine: CoA ligase (CaiC) in the activation of betaines and the transfer of coenzyme A in Escherichia coli . . J Appl Microbiol 105:, 42–50. [CrossRef] [PubMed]
    [Google Scholar]
  14. Beumer R. R. , Te Giffel M. C. , Cox L. J. , Rombouts F. M. , Abee T. . ( 1994;). Effect of exogenous proline, betaine, and carnitine on growth of Listeria monocytogenes in a minimal medium. . Appl Environ Microbiol 60:, 1359–1363. [CrossRef] [PubMed]
    [Google Scholar]
  15. Bieber L. L. . ( 1988;). Carnitine. . Annu Rev Biochem 57:, 261–283. [CrossRef] [PubMed]
    [Google Scholar]
  16. Bremer J. . ( 1983;). Carnitine – metabolism and functions. . Physiol Rev 63:, 1420–1480. [PubMed]
    [Google Scholar]
  17. Bremer E. . ( 2011;). Crystal ball – 2011. . Environ Microbiol Rep 3:, 1–26. [CrossRef] [PubMed]
    [Google Scholar]
  18. Brown A. D. , Simpson J. R. . ( 1972;). Water relations of sugar-tolerant yeasts: the role of intracellular polyols. . J Gen Microbiol 72:, 589–591. [CrossRef] [PubMed]
    [Google Scholar]
  19. Buchet A. , Eichler K. , Mandrand-Berthelot M. A. . ( 1998;). Regulation of the carnitine pathway in Escherichia coli: investigation of the caifix divergent promoter region. . J Bacteriol 180:, 2599–2608. [PubMed]
    [Google Scholar]
  20. Buchet A. , Nasser W. , Eichler K. , Mandrand-Berthelot M. A. . ( 1999;). Positive co-regulation of the Escherichia coli carnitine pathway cai and fix operons by CRP and the CaiF activator. . Mol Microbiol 34:, 562–575. [CrossRef]
    [Google Scholar]
  21. Canovas D. , Castellar M. R. , Obon T. , Torroglosa C. , Olivares J. L. , Iborra J. L. . ( 2003;). Racemisation of d(+)-carnitine into l( − )-carnitine by Escherichia coli strains. . Process Biochem 39:, 287–293. [CrossRef]
    [Google Scholar]
  22. Castellar M. R. , Cánovas M. , Kleber H. P. , Iborra J. L. . ( 1998;). Biotransformation of d(+)-carnitine into l( − )-carnitine by resting cells of Escherichia coli O44 K74. . J Appl Microbiol 85:, 883–890. [CrossRef] [PubMed]
    [Google Scholar]
  23. Cave M. C. , Hurt R. T. , Frazier T. H. , Matheson P. J. , Garrison R. N. , McClain C. J. , McClave S. A. . ( 2008;). Obesity, inflammation, and the potential application of pharmaconutrition. . Nutr Clin Pract 23:, 16–34. [CrossRef] [PubMed]
    [Google Scholar]
  24. Chen C. , Beattie G. A. . ( 2007;). Characterization of the osmoprotectant transporter OpuC from Pseudomonas syringae and demonstration that cystathionine-beta-synthase domains are required for its osmoregulatory function. . J Bacteriol 189:, 6901–6912. [CrossRef] [PubMed]
    [Google Scholar]
  25. Chen C. , Malek A. A. , Wargo M. J. , Hogan D. A. , Beattie G. A. . ( 2010;). The ATP-binding cassette transporter Cbc (choline/betaine/carnitine) recruits multiple substrate-binding proteins with strong specificity for distinct quaternary ammonium compounds. . Mol Microbiol 75:, 29–45. [CrossRef] [PubMed]
    [Google Scholar]
  26. Combs G. F. Jr . ( 2012;). The Vitamins: Fundamental Aspects in Health and Nutrition, , 4th edn.. London:: Academic Press;.
    [Google Scholar]
  27. Creasey E. A. , Delahay R. M. , Daniell S. J. , Frankel G. . ( 2003;). Yeast two-hybrid system survey of interactions between LEE-encoded proteins of enteropathogenic Escherichia coli . . Microbiology 149:, 2093–2106. [CrossRef] [PubMed]
    [Google Scholar]
  28. Curson A. R. , Todd J. D. , Sullivan M. J. , Johnston A. W. . ( 2011;). Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. . Nat Rev Microbiol 9:, 849–859. [CrossRef] [PubMed]
    [Google Scholar]
  29. Dalmastri C. , Fiore A. , Alisi C. , Bevivino A. , Tabacchioni S. , Giuliano G. , Sprocati A. R. , Segre L. , Mahenthiralingam E. , other authors . ( 2003;). A rhizospheric Burkholderia cepacia complex population: genotypic and phenotypic diversity of Burkholderia cenocepacia and Burkholderia ambifaria . . FEMS Microbiol Ecol 46:, 179–187. [CrossRef] [PubMed]
    [Google Scholar]
  30. Du Y. , Shi W. W. , He Y. X. , Yang Y. H. , Zhou C. Z. , Chen Y. . ( 2011;). Structures of the substrate-binding protein provide insights into the multiple compatible solute binding specificities of the Bacillus subtilis ABC transporter OpuC. . Biochem J 436:, 283–289. [CrossRef] [PubMed]
    [Google Scholar]
  31. Eichler K. , Schunck W. H. , Kleber H. P. , Mandrand-Berthelot M. A. . ( 1994a;). Cloning, nucleotide sequence, and expression of the Escherichia coli gene encoding carnitine dehydratase. . J Bacteriol 176:, 2970–2975. [CrossRef] [PubMed]
    [Google Scholar]
  32. Eichler K. , Bourgis F. , Buchet A. , Kleber H. P. , Mandrand-Berthelot M. A. . ( 1994b;). Molecular characterization of the cai operon necessary for carnitine metabolism in Escherichia coli . . Mol Microbiol 13:, 775–786. [CrossRef] [PubMed]
    [Google Scholar]
  33. Eichler K. , Buchet A. , Bourgis F. , Kleber H. P. , Mandrand-Berthelot M. A. . ( 1995;). The fix Escherichia coli region contains four genes related to carnitine metabolism. . J Basic Microbiol 35:, 217–227. [CrossRef] [PubMed]
    [Google Scholar]
  34. Eichler K. , Buchet A. , Lemke R. , Kleber H. P. , Mandrand-Berthelot M. A. . ( 1996;). Identification and characterization of the caiF gene encoding a potential transcriptional activator of carnitine metabolism in Escherichia coli . . J Bacteriol 178:, 1248–1257. [CrossRef] [PubMed]
    [Google Scholar]
  35. Elssner T. , Preusser A. , Wagner U. , Kleber H. P. . ( 1999;). Metabolism of l( − )-carnitine by Enterobacteriaceae under aerobic conditions. . FEMS Microbiol Lett 174:, 295–301. [CrossRef] [PubMed]
    [Google Scholar]
  36. Elssner T. , Hennig L. , Frauendorf H. , Haferburg D. , Kleber H. P. . ( 2000;). Isolation, identification, and synthesis of gamma-butyrobetainyl-CoA and crotonobetainyl-CoA, compounds involved in carnitine metabolism of E. coli . . Biochemistry 39:, 10761–10769. [CrossRef] [PubMed]
    [Google Scholar]
  37. Elssner T. , Engemann C. , Baumgart K. , Kleber H. P. . ( 2001;). Involvement of coenzyme A esters and two new enzymes, an enoyl-CoA hydratase and a CoA-transferase, in the hydration of crotonobetaine to l-carnitine by Escherichia coli . . Biochemistry 40:, 11140–11148. [CrossRef] [PubMed]
    [Google Scholar]
  38. Engemann C. , Kleber H. P. . ( 2001;). Epigenetic regulation of carnitine metabolising enzymes in Proteus sp. under aerobic conditions. . FEMS Microbiol Lett 196:, 1–6. [CrossRef] [PubMed]
    [Google Scholar]
  39. Engemann C. , Elssner T. , Kleber H. P. . ( 2001;). Biotransformation of crotonobetaine to l( − )-carnitine in Proteus sp. . Arch Microbiol 175:, 353–359. [CrossRef] [PubMed]
    [Google Scholar]
  40. Engemann C. , Elssner T. , Pfeifer S. , Krumbholz C. , Maier T. , Kleber H. P. . ( 2005;). Identification and functional characterisation of genes and corresponding enzymes involved in carnitine metabolism of Proteus sp. . Arch Microbiol 183:, 176–189. [CrossRef] [PubMed]
    [Google Scholar]
  41. Fitzsimmons L. F. , Hampel K. J. , Wargo M. J. . ( 2012;). Cellular choline and glycine betaine pools impact osmoprotection and phospholipase C production in Pseudomonas aeruginosa . . J Bacteriol 194:, 4718–4726. [CrossRef] [PubMed]
    [Google Scholar]
  42. Flanagan J. L. , Simmons P. A. , Vehige J. , Willcox M. D. , Garrett Q. . ( 2010;). Role of carnitine in disease. . Nutr Metab (Lond) 7:, 30. [CrossRef] [PubMed]
    [Google Scholar]
  43. Fraenkel G. , Friedman S. . ( 1957;). Carnitine. . Vitam Horm 15:, 73–118. [CrossRef] [PubMed]
    [Google Scholar]
  44. Fraser K. R. , O'Byrne C. P. . ( 2002;). Osmoprotection by carnitine in a Listeria monocytogenes mutant lacking the OpuC transporter: evidence for a low affinity carnitine uptake system. . FEMS Microbiol Lett 211:, 189–194. [CrossRef] [PubMed]
    [Google Scholar]
  45. Fraser C. M. , Norris S. J. , Weinstock G. M. , White O. , Sutton G. G. , Dodson R. , Gwinn M. , Hickey E. K. , Clayton R. , other authors . ( 1998;). Complete genome sequence of Treponema pallidum, the syphilis spirochete. . Science 281:, 375–388. [CrossRef] [PubMed]
    [Google Scholar]
  46. Fraser K. R. , Harvie D. , Coote P. J. , O'Byrne C. P. . ( 2000;). Identification and characterization of an ATP binding cassette l-carnitine transporter in Listeria monocytogenes . . Appl Environ Microbiol 66:, 4696–4704. [CrossRef] [PubMed]
    [Google Scholar]
  47. Gahan C. G. , Hill C. . ( 2014;). Listeria monocytogenes: survival and adaptation in the gastrointestinal tract. . Front Cell Infect Microbiol 4:, 9. [CrossRef] [PubMed]
    [Google Scholar]
  48. Goldmann A. , Boivin C. , Fleury V. , Message B. , Lecoeur L. , Maille M. , Tepfer D. . ( 1991;). Betaine use by rhizosphere bacteria: genes essential for trigonelline, stachydrine, and carnitine catabolism in Rhizobium meliloti are located on pSym in the symbiotic region. . Mol Plant Microbe Interact 4:, 571–578. [CrossRef] [PubMed]
    [Google Scholar]
  49. Gulewitsch W. , Krimberg R. . ( 1905;). [On carnitine]. . Hoppe Seylers Z Physiol Chem 45:, 326–330 (in German). [CrossRef]
    [Google Scholar]
  50. Hanschmann H. , Kleber H. P. . ( 1997;). Purification and characterization of d(+)-carnitine dehydrogenase from Agrobacterium sp. – a new enzyme of carnitine metabolism. . Biochim Biophys Acta 1337:, 133–142. [CrossRef] [PubMed]
    [Google Scholar]
  51. Hanschmann H. , Ehricht R. , Kleber H. P. . ( 1996;). Purification and properties of l( − )-carnitine dehydrogenase from Agrobacterium sp. . Biochim Biophys Acta 1290:, 177–183. [CrossRef] [PubMed]
    [Google Scholar]
  52. Hartiala J. , Bennett B. J. , Tang W. H. , Wang Z. , Stewart A. F. , Roberts R. , McPherson R. , Lusis A. J. , Hazen S. L. , Allayee H. , CARDIoGRAM Consortium . ( 2014;). Comparative genome-wide association studies in mice and humans for trimethylamine N-oxide, a proatherogenic metabolite of choline and l-carnitine. . Arterioscler Thromb Vasc Biol 34:, 1307–1313. [CrossRef] [PubMed]
    [Google Scholar]
  53. Hoffmann T. , Bremer E. . ( 2011;). Protection of Bacillus subtilis against cold stress via compatible-solute acquisition. . J Bacteriol 193:, 1552–1562. [CrossRef] [PubMed]
    [Google Scholar]
  54. Hoffmann T. , Wensing A. , Brosius M. , Steil L. , Völker U. , Bremer E. . ( 2013;). Osmotic control of opuA expression in Bacillus subtilis and its modulation in response to intracellular glycine betaine and proline pools. . J Bacteriol 195:, 510–522. [CrossRef] [PubMed]
    [Google Scholar]
  55. Hung K. , Kleber H. P. . ( 1985;). [Occurrence and regulation of carnitine dehydrogenase of Pseudomonas species]. . Wiss Z Karl-Marx-Univ Leipzig Math-Nat R 34:, 293–296 (in German).
    [Google Scholar]
  56. Hwang K. C. , Bang W. . ( 1997;). Optimal resolution of l-carnitine from racemic dl-carnitine by Enterobacter sp. assimilating d-carnitine. . J Microbiol Biotechnol 7:, 318–322.
    [Google Scholar]
  57. Ivanova E. P. , Gorshkova N. M. , Bowman J. P. , Lysenko A. M. , Zhukova N. V. , Sergeev A. F. , Mikhailov V. V. , Nicolau D. V. . ( 2004;). Shewanella pacifica sp. nov., a polyunsaturated fatty acid-producing bacterium isolated from sea water. . Int J Syst Evol Microbiol 54:, 1083–1087. [CrossRef] [PubMed]
    [Google Scholar]
  58. Jaenicke R. , Heber U. , Franks F. , Chapman D. , Griffin M. C. A. , Hvidt A. , Cowan D. A. . ( 1990;). Protein structure and function at low temperatures. . Philos Trans R Soc Lond B Biol Sci 326:, 535–551. [CrossRef] [PubMed]
    [Google Scholar]
  59. Jebbar M. , Champion C. , Blanco C. , Bonnassie S. . ( 1998;). Carnitine acts as a compatible solute in Brevibacterium linens . . Res Microbiol 149:, 211–219. [CrossRef] [PubMed]
    [Google Scholar]
  60. Joeres U. , Kula M. R. . ( 1994;). Purification and characterisation of a microbial l-carnitine amidase. . Appl Microbiol Biotechnol 40:, 606–610. [CrossRef] [PubMed]
    [Google Scholar]
  61. Johri A. M. , Heyland D. K. , Hétu M. F. , Crawford B. , Spence J. D. . ( 2014;). Carnitine therapy for the treatment of metabolic syndrome and cardiovascular disease: evidence and controversies. . Nutr Metab Cardiovasc Dis 24:, 808–814. [CrossRef] [PubMed]
    [Google Scholar]
  62. Jung H. , Kleber H. P. . ( 1991;). Metabolism of d(+)carnitine by Escherichia coli . . Appl Microbiol Biotechnol 35:, 391–395. [CrossRef]
    [Google Scholar]
  63. Jung K. , Jung H. , Kleber H. P. . ( 1987;). Regulation of l-carnitine metabolism in Escherichia coli . . J Basic Microbiol 27:, 131–137. [CrossRef] [PubMed]
    [Google Scholar]
  64. Jung H. , Jung K. , Kleber H. P. . ( 1989;). Purification and properties of carnitine dehydratase from Escherichia coli – a new enzyme of carnitine metabolization. . Biochim Biophys Acta 1003:, 270–276. [CrossRef] [PubMed]
    [Google Scholar]
  65. Jung H. , Jung K. , Kleber H. P. . ( 1990;). l-Carnitine uptake by Escherichia coli . . J Basic Microbiol 30:, 507–514. [CrossRef] [PubMed]
    [Google Scholar]
  66. Jung H. , Buchholz M. , Clausen J. , Nietschke M. , Revermann A. , Schmid R. , Jung K. . ( 2002;). CaiT of Escherichia coli, a new transporter catalyzing l-carnitine/gamma-butyrobetaine exchange. . J Biol Chem 277:, 39251–39258. [CrossRef] [PubMed]
    [Google Scholar]
  67. Kakayama K. , Honda H. , Ogawa Y. , Ohta T. , Ozawa T. . ( 1991;). Method of producing carnitine. ., US Patent 5,041,375.
  68. Kalayil S. , Schulze S. , Kühlbrandt W. . ( 2013;). Arginine oscillation explains Na+ independence in the substrate/product antiporter CaiT. . Proc Natl Acad Sci U S A 110:, 17296–17301. [CrossRef] [PubMed]
    [Google Scholar]
  69. Kappes R. M. , Bremer E. . ( 1998;). Response of Bacillus subtilis to high osmolarity: uptake of carnitine, crotonobetaine and γ-butyrobetaine via the ABC transport system OpuC. . Microbiology 144:, 83–90. [CrossRef]
    [Google Scholar]
  70. Kelley L. A. , Sternberg M. J. . ( 2009;). Protein structure prediction on the Web: a case study using the Phyre server. . Nat Protoc 4:, 363–371. [CrossRef] [PubMed]
    [Google Scholar]
  71. Kets E. P. W. , Galinski E. A. , de Bont J. A. M. . ( 1994;). Carnitine: a novel compatible solute in Lactobacillus plantarum . . Arch Microbiol 162:, 243–248. [CrossRef]
    [Google Scholar]
  72. Klagsbrun M. , Furano A. V. . ( 1975;). Methylated amino acids in the proteins of bacterial and mammalian cells. . Arch Biochem Biophys 169:, 529–539. [CrossRef] [PubMed]
    [Google Scholar]
  73. Kleber H. P. . ( 1997;). Bacterial carnitine metabolism. . FEMS Microbiol Lett 147:, 1–9. [CrossRef] [PubMed]
    [Google Scholar]
  74. Kleber H. P. , Aurich H. . ( 1967;). [Damped oscillations in the synthesis of carnitine dehydrogenase by Pseudomonas aeruginosa]. . Hoppe Seylers Z Physiol Chem 348:, 1727–1729 (in German). [PubMed]
    [Google Scholar]
  75. Kleber H. P. , Schöpp W. , Sorger H. , Tauchert H. , Aurich H. . ( 1967;). [Formation of 3-dehydrocarnitine from l-carnitine through the action of a Pseudomonas aeruginosa enzyme]. . Acta Biol Med Ger 19:, 659–667 (in German). [PubMed]
    [Google Scholar]
  76. Kleber H. P. , Seim H. , Aurich H. , Strack E. . ( 1977;). [Utilization of trimethylammonium-compounds by Acinetobacter calcoaceticus (author's transl)]. . Arch Microbiol 112:, 201–206 (in German). [CrossRef] [PubMed]
    [Google Scholar]
  77. Kleber H. P. , Seim H. , Aurich H. , Strack E. . ( 1978;). [Interrelationships between carnitine metabolism and fatty acid assimilation in Pseudomonas putida (author's transl)]. . Arch Microbiol 116:, 213–220 (in German). [CrossRef] [PubMed]
    [Google Scholar]
  78. Klüttermann K. , Tauchert H. , Kleber H. P. . ( 2002;). Synthesis of poly-beta-hydroxybutyrate by Agrobacterium radiobacter after growth on d-carnitine. . Acta Biotechnol 22:, 261–269. [CrossRef]
    [Google Scholar]
  79. Koeth R. A. , Wang Z. , Levison B. S. , Buffa J. A. , Org E. , Sheehy B. T. , Britt E. B. , Fu X. , Wu Y. , other authors . ( 2013;). Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. . Nat Med 19:, 576–585. [CrossRef] [PubMed]
    [Google Scholar]
  80. Kuka J. , Liepinsh E. , Makrecka-Kuka M. , Liepins J. , Cirule H. , Gustina D. , Loza E. , Zharkova-Malkova O. , Grinberga S. , other authors . ( 2014;). Suppression of intestinal microbiota-dependent production of pro-atherogenic trimethylamine N-oxide by shifting l-carnitine microbial degradation. . Life Sci 117:, 84–92. [CrossRef] [PubMed]
    [Google Scholar]
  81. Kula M. R. , Joeres U. . ( 1993;). l-Carnitine amidase produced by a microorganism. ., US Patent 5,238,838.
  82. Kula M. R. , Joeres U. , Stelkes-Ritter U. . ( 1996;). New microbial amidases. . Ann N Y Acad Sci 799:, 725–728. [CrossRef]
    [Google Scholar]
  83. Kutscher F. . ( 1905;). [Zur Kenntnis des Novains]. . Hoppe-Seyler's Z Physiol Chem 49:, 47–49 (in German).[CrossRef]
    [Google Scholar]
  84. Lindstedt G. , Lindstedt S. . ( 1970;). Cofactor requirements of gamma-butyrobetaine hydroxylase from rat liver. . J Biol Chem 245:, 4178–4186. [PubMed]
    [Google Scholar]
  85. Lindstedt G. , Lindstedt S. , Midtvedt T. , Tofft M. . ( 1967;). The formation and degradation of carnitine in Pseudomonas . . Biochemistry 6:, 1262–1270. [CrossRef]
    [Google Scholar]
  86. Lindstedt G. , Lindstedt S. , Olander B. , Tofft M. . ( 1968;). Alpha-ketoglutarate and hydroxylation of gamma-butyrobetaine. . Biochim Biophys Acta 158:, 503–505. [PubMed] [CrossRef]
    [Google Scholar]
  87. Lindstedt G. , Lindstedt S. , Tofft M. . ( 1970a;). Gamma-butyrobetaine hydroxylase from Pseudomonas sp AK 1. . Biochemistry 9:, 4336–4342. [PubMed] [CrossRef]
    [Google Scholar]
  88. Lindstedt G. , Lindstedt S. , Midtvedt T. , Tofft M. . ( 1970b;). Inducible gamma-butyrobetaine-degrading enzymes in Pseudomonas species AK 1. . J Bacteriol 101:, 1094–1095. [CrossRef] [PubMed]
    [Google Scholar]
  89. Lu X. , Zhang P. , Li Q. , Liu H. , Lin X. , Ma X. . ( 2012;). [Cloning, expression and characterization of a gamma-butyrobetaine hydroxylase gene bbh from Pseudomonas sp. L-1]. . Wei Sheng Wu Xue Bao 52:, 602–610 (in Chinese). [CrossRef] [PubMed]
    [Google Scholar]
  90. Lucchesi G. I. , Lisa T. A. , Casale C. H. , Domenech C. E. . ( 1995;). Carnitine resembles choline in the induction of cholinesterase, acid phosphatase, and phospholipase C and in its action as an osmoprotectant in Pseudomonas aeruginosa . . Curr Microbiol 30:, 55–60. [CrossRef] [PubMed]
    [Google Scholar]
  91. Malek A. A. , Chen C. , Wargo M. J. , Beattie G. A. , Hogan D. A. . ( 2011;). Roles of three transporters, CbcXWV, BetT1, and BetT3, in Pseudomonas aeruginosa choline uptake for catabolism. . J Bacteriol 193:, 3033–3041. [CrossRef] [PubMed]
    [Google Scholar]
  92. Marciani P. , Lindi C. , Marzo A. , Arrigoni Martelli E. , Cardace G. , Esposito G. . ( 1991;). l-Carnitine and carnitine ester transport in the rat small intestine. . Pharmacol Res 23:, 157–162. [CrossRef] [PubMed]
    [Google Scholar]
  93. Meadows J. A. , Wargo M. J. . ( 2013;). Characterization of Pseudomonas aeruginosa growth on O-acylcarnitines and identification of a short-chain acylcarnitine hydrolase. . Appl Environ Microbiol 79:, 3355–3363. [CrossRef] [PubMed]
    [Google Scholar]
  94. Miller T. R. , Hnilicka K. , Dziedzic A. , Desplats P. , Belas R. . ( 2004;). Chemotaxis of Silicibacter sp. strain TM1040 toward dinoflagellate products. . Appl Environ Microbiol 70:, 4692–4701. [CrossRef] [PubMed]
    [Google Scholar]
  95. Miura-Fraboin J. , Kleber H. P. , Englard S. . ( 1982;). Assimilation of gamma-butyrobetaine, and d- and l-carnitine by resting cell suspensions of Acinetobacter calcoaceticus and Pseudomonas putida . . Arch Microbiol 133:, 217–221. [CrossRef]
    [Google Scholar]
  96. Monnich K. , Hanschmann H. , Kleber H. P. . ( 1995;). Utilization of d-carnitine by Pseudomonas sp. AK 1. . FEMS Microbiol Lett 132:, 51–55. [CrossRef]
    [Google Scholar]
  97. Mori N. , Kasugai T. , Kitamoto Y. , Ichikawa Y. . ( 1988;). Purification and some properties of carnitine dehydrogenase from Xanthomonas translucens . . Agric Biol Chem 52:, 249–250. [CrossRef]
    [Google Scholar]
  98. Naidu G. S. , Lee I. Y. , Cho O. K. , Park Y. H. . ( 2001;). Conversion of gamma-butyrobetaine to l-carnitine by Achromobacter cycloclast . . J Ind Microbiol Biotechnol 26:, 309–315. [CrossRef] [PubMed]
    [Google Scholar]
  99. Nguyen U. T. , Wenderska I. B. , Chong M. A. , Koteva K. , Wright G. D. , Burrows L. L. . ( 2012;). Small-molecule modulators of Listeria monocytogenes biofilm development. . Appl Environ Microbiol 78:, 1454–1465. [CrossRef] [PubMed]
    [Google Scholar]
  100. Nobile S. , Deshusses J. . ( 1986;). Transport of gamma-butyrobetaine in an Agrobacterium species isolated from soil. . J Bacteriol 168:, 780–784. [PubMed]
    [Google Scholar]
  101. Obón J. M. , Maiquez J. R. , Cánovas M. , Kleber H. P. , Iborra J. L. . ( 1999;). High-density Escherichia coli cultures for continuous l( − )-carnitine production. . Appl Microbiol Biotechnol 51:, 760–764. [CrossRef] [PubMed]
    [Google Scholar]
  102. Palmer G. C. , Jorth P. A. , Whiteley M. . ( 2013;). The role of two Pseudomonas aeruginosa anthranilate synthases in tryptophan and quorum signal production. . Microbiology 159:, 959–969. [CrossRef] [PubMed]
    [Google Scholar]
  103. Park S. , Smith L. T. , Smith G. M. . ( 1995;). Role of glycine betaine and related osmolytes in osmotic stress adaptation in Yersinia enterocolitica ATCC 9610. . Appl Environ Microbiol 61:, 4378–4381. [PubMed]
    [Google Scholar]
  104. Preusser A. , Wagner U. , Elssner T. , Kleber H. P. . ( 1999;). Crotonobetaine reductase from Escherichia coli consists of two proteins. . Biochim Biophys Acta 1431:, 166–178. [CrossRef] [PubMed]
    [Google Scholar]
  105. Privalov P. L. , Gill S. J. . ( 1988;). Stability of protein structure and hydrophobic interaction. . Adv Protein Chem 39:, 191–234. [CrossRef] [PubMed]
    [Google Scholar]
  106. Rebouche C. J. . ( 2004;). Kinetics, pharmacokinetics, and regulation of l-carnitine and acetyl-l-carnitine metabolism. . Ann N Y Acad Sci 1033:, 30–41. [CrossRef] [PubMed]
    [Google Scholar]
  107. Rebouche C. J. . ( 2014;). Modern Nutrition in Health and Disease, , 11th edn.. Baltimore, MD:: Lippincott Williams & Wilkins;.
    [Google Scholar]
  108. Rebouche C. J. , Chenard C. A. . ( 1991;). Metabolic fate of dietary carnitine in human adults: identification and quantification of urinary and fecal metabolites. . J Nutr 121:, 539–546. [PubMed]
    [Google Scholar]
  109. Rebouche C. J. , Seim H. . ( 1998;). Carnitine metabolism and its regulation in microorganisms and mammals. . Annu Rev Nutr 18:, 39–61. [CrossRef] [PubMed]
    [Google Scholar]
  110. Reddy J. K. , Hashimoto T. . ( 2001;). Peroxisomal beta-oxidation and peroxisome proliferator-activated receptor alpha: an adaptive metabolic system. . Annu Rev Nutr 21:, 193–230. [CrossRef] [PubMed]
    [Google Scholar]
  111. Robert H. , Le Marrec C. , Blanco C. , Jebbar M. . ( 2000;). Glycine betaine, carnitine, and choline enhance salinity tolerance and prevent the accumulation of sodium to a level inhibiting growth of Tetragenococcus halophila . . Appl Environ Microbiol 66:, 509–517. [CrossRef] [PubMed]
    [Google Scholar]
  112. Roth S. , Jung K. , Jung H. , Hommel R. K. , Kleber H. P. . ( 1994;). Crotonobetaine reductase from Escherichia coli – a new inducible enzyme of anaerobic metabolization of l( − )-carnitine. . Antonie van Leeuwenhoek 65:, 63–69. [CrossRef] [PubMed]
    [Google Scholar]
  113. Rudolph A. S. , Crowe J. H. , Crowe L. M. . ( 1986;). Effects of three stabilizing agents – proline, betaine, and trehalose – on membrane phospholipids. . Arch Biochem Biophys 245:, 134–143. [CrossRef] [PubMed]
    [Google Scholar]
  114. Rüetschi U. , Nordin I. , Odelhög B. , Jörnvall H. , Lindstedt S. . ( 1993;). γ-Butyrobetaine hydroxylase. Structural characterization of the Pseudomonas enzyme. . Eur J Biochem 213:, 1075–1080. [CrossRef] [PubMed]
    [Google Scholar]
  115. Russell R. M. , Sharp F. C. , Rasko D. A. , Sperandio V. . ( 2007;). QseA and GrlR/GrlA regulation of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli . . J Bacteriol 189:, 5387–5392. [CrossRef] [PubMed]
    [Google Scholar]
  116. Ryser E. T. , Marth E. H. . ( 2007;). Listeria, Listeriosis, and Food Safety, , 3rd edn.. Boca Raton, FL:: CRC Press;.[CrossRef]
    [Google Scholar]
  117. Saier M. H. Jr , Paulsen I. T. . ( 2000;). Whole genome analyses of transporters in spirochetes: Borrelia burgdorferi and Treponema pallidum . . J Mol Microbiol Biotechnol 2:, 393–399.[PubMed]
    [Google Scholar]
  118. Schiefner A. , Breed J. , Bösser L. , Kneip S. , Gade J. , Holtmann G. , Diederichs K. , Welte W. , Bremer E. . ( 2004;). Cation–pi interactions as determinants for binding of the compatible solutes glycine betaine and proline betaine by the periplasmic ligand-binding protein ProX from Escherichia coli . . J Biol Chem 279:, 5588–5596. [CrossRef] [PubMed]
    [Google Scholar]
  119. Schulze S. , Köster S. , Geldmacher U. , Terwisscha van Scheltinga A. C. , Kühlbrandt W. . ( 2010;). Structural basis of Na+-independent and cooperative substrate/product antiport in CaiT. . Nature 467:, 233–236. [CrossRef] [PubMed]
    [Google Scholar]
  120. Seim H. , Löster H. , Claus R. , Kleber H. P. , Strack E. . ( 1982a;). Stimulation of the anaerobic growth of Salmonella typhimurium by reduction of l-carnitine, carnitine derivatives and structure-related trimethylammonium compounds. . Arch Microbiol 132:, 91–95. [CrossRef] [PubMed]
    [Google Scholar]
  121. Seim H. , Loster H. , Claus R. , Kleber H. P. , Strack E. . ( 1982b;). Formation of gamma-butryobetaine and trimethylamine from quaternary ammonium compounds structure-related to l-carnitine and choline by Proteus vularis . . FEMS Microbiol Lett 13:, 201–205.
    [Google Scholar]
  122. Seim H. , Loster H. , Kleber H. P. . ( 1982c;). [Reductive metabolism of l-carnitine and structure-related trimethylammonium compounds in Escherichia coli]. . Acta Biol Med Ger 41:, 1009–1019 (in German). [PubMed]
    [Google Scholar]
  123. Seymour J. R. , Simó R. , Ahmed T. , Stocker R. . ( 2010;). Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. . Science 329:, 342–345. [CrossRef] [PubMed]
    [Google Scholar]
  124. Sikorski J. , Stackebrandt E. , Wackernagel W. . ( 2001;). Pseudomonas kilonensis sp. nov., a bacterium isolated from agricultural soil. . Int J Syst Evol Microbiol 51:, 1549–1555. [PubMed]
    [Google Scholar]
  125. Sleator R. D. , Hill C. . ( 2010;). Compatible solutes: the key to Listeria's success as a versatile gastrointestinal pathogen?. Gut Pathog 2:, 20. [CrossRef] [PubMed]
    [Google Scholar]
  126. Sleator R. D. , Wouters J. , Gahan C. G. , Abee T. , Hill C. . ( 2001;). Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes . . Appl Environ Microbiol 67:, 2692–2698. [CrossRef] [PubMed]
    [Google Scholar]
  127. Sleator R. D. , Francis G. A. , O'Beirne D. , Gahan C. G. , Hill C. . ( 2003;). Betaine and carnitine uptake systems in Listeria monocytogenes affect growth and survival in foods and during infection. . J Appl Microbiol 95:, 839–846. [CrossRef] [PubMed]
    [Google Scholar]
  128. Sleator R. D. , Banville N. , Hill C. . ( 2009;). Carnitine enhances the growth of Listeria monocytogenes in infant formula at 7 degrees C. . J Food Prot 72:, 1293–1295. [PubMed]
    [Google Scholar]
  129. Smajs D. , McKevitt M. , Howell J. K. , Norris S. J. , Cai W. W. , Palzkill T. , Weinstock G. M. . ( 2005;). Transcriptome of Treponema pallidum: gene expression profile during experimental rabbit infection. . J Bacteriol 187:, 1866–1874. [CrossRef] [PubMed]
    [Google Scholar]
  130. Smiddy M. , Sleator R. D. , Patterson M. F. , Hill C. , Kelly A. L. . ( 2004;). Role for compatible solutes glycine betaine and l-carnitine in listerial barotolerance. . Appl Environ Microbiol 70:, 7555–7557. [CrossRef] [PubMed]
    [Google Scholar]
  131. Steiber A. , Kerner J. , Hoppel C. L. . ( 2004;). Carnitine: a nutritional, biosynthetic, and functional perspective. . Mol Aspects Med 25:, 455–473. [CrossRef] [PubMed]
    [Google Scholar]
  132. Stocker R. , Seymour J. R. . ( 2012;). Ecology and physics of bacterial chemotaxis in the ocean. . Microbiol Mol Biol Rev 76:, 792–812. [CrossRef] [PubMed]
    [Google Scholar]
  133. Strøm A. R. , Olafsen J. A. , Larsen H. . ( 1979;). Trimethylamine oxide: a terminal electron acceptor in anaerobic respiration of bacteria. . J Gen Microbiol 112:, 315–320. [CrossRef] [PubMed]
    [Google Scholar]
  134. Takahashi M. , Ueda S. . ( 1995;). Method of assaying for acyl-l-carnitine and short-chain acyl-carnitine. ., US Patent 5,385,829.
  135. Tang L. , Bai L. , Wang W. H. , Jiang T. . ( 2010;). Crystal structure of the carnitine transporter and insights into the antiport mechanism. . Nat Struct Mol Biol 17:, 492–496. [CrossRef] [PubMed]
    [Google Scholar]
  136. Tars K. , Leitans J. , Kazaks A. , Zelencova D. , Liepinsh E. , Kuka J. , Makrecka M. , Lola D. , Andrianovs V. , other authors . ( 2014;). Targeting carnitine biosynthesis: discovery of new inhibitors against γ-butyrobetaine hydroxylase. . J Med Chem 57:, 2213–2236. [CrossRef] [PubMed]
    [Google Scholar]
  137. Uanschou C. , Frieht R. , Pittner F. . ( 2005;). What to learn from comparative genomic sequence analysis of l-carnitine dehydrogenase. . Monatsh Chem 136:, 1365–1381. [CrossRef]
    [Google Scholar]
  138. Unemoto T. , Hayashi M. , Miyaki K. , Hayashi M. . ( 1966;). Formation of trimethylamine from dl-carnitine by Serratia marcescens . . Biochim Biophys Acta 121:, 220–222. [CrossRef] [PubMed]
    [Google Scholar]
  139. Ussher J. R. , Lopaschuk G. D. , Arduini A. . ( 2013;). Gut microbiota metabolism of l-carnitine and cardiovascular risk. . Atherosclerosis 231:, 456–461. [CrossRef] [PubMed]
    [Google Scholar]
  140. Vaz F. M. , Wanders R. J. . ( 2002;). Carnitine biosynthesis in mammals. . Biochem J 361:, 417–429. [CrossRef] [PubMed]
    [Google Scholar]
  141. Verheul A. , Rombouts F. M. , Beumer R. R. , Abee T. . ( 1995;). An ATP-dependent l-carnitine transporter in Listeria monocytogenes Scott A is involved in osmoprotection. . J Bacteriol 177:, 3205–3212. [PubMed]
    [Google Scholar]
  142. Verheul A. , Glaasker E. , Poolman B. , Abee T. . ( 1997;). Betaine and l-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals. . J Bacteriol 179:, 6979–6985. [PubMed]
    [Google Scholar]
  143. Verheul A. , Wouters J. A. , Rombouts F. M. , Abee T. . ( 1998;). A possible role of ProP, ProU and CaiT in osmoprotection of Escherichia coli by carnitine. . J Appl Microbiol 85:, 1036–1046. [CrossRef] [PubMed]
    [Google Scholar]
  144. Vilhelmsson O. , Miller K. J. . ( 2002;). Humectant permeability influences growth and compatible solute uptake by Staphylococcus aureus subjected to osmotic stress. . J Food Prot 65:, 1008–1015. [PubMed]
    [Google Scholar]
  145. Walt A. , Kahn M. L. . ( 2002;). The fixA and fixB genes are necessary for anaerobic carnitine reduction in Escherichia coli . . J Bacteriol 184:, 4044–4047. [CrossRef] [PubMed]
    [Google Scholar]
  146. Wanders R. J. , Waterham H. R. . ( 2006;). Biochemistry of mammalian peroxisomes revisited. . Annu Rev Biochem 75:, 295–332. [CrossRef] [PubMed]
    [Google Scholar]
  147. Wargo M. J. . ( 2013;). Homeostasis and catabolism of choline and glycine betaine: lessons from Pseudomonas aeruginosa . . Appl Environ Microbiol 79:, 2112–2120. [CrossRef] [PubMed]
    [Google Scholar]
  148. Wargo M. J. , Hogan D. A. . ( 2009;). Identification of genes required for Pseudomonas aeruginosa carnitine catabolism. . Microbiology 155:, 2411–2419. [CrossRef] [PubMed]
    [Google Scholar]
  149. Wargo M. J. , Szwergold B. S. , Hogan D. A. . ( 2008;). Identification of two gene clusters and a transcriptional regulator required for Pseudomonas aeruginosa glycine betaine catabolism. . J Bacteriol 190:, 2690–2699. [CrossRef] [PubMed]
    [Google Scholar]
  150. Warren C. R. . ( 2013a;). High diversity of small organic N observed in soil water. . Soil Biol Biochem 57:, 444–450. [CrossRef]
    [Google Scholar]
  151. Warren C. R. . ( 2013b;). Quaternary ammonium compounds can be abundant in some soils and are taken up as intact molecules by plants. . New Phytol 198:, 476–485. [CrossRef] [PubMed]
    [Google Scholar]
  152. Watson D. , Sleator R. D. , Casey P. G. , Hill C. , Gahan C. G. . ( 2009;). Specific osmolyte transporters mediate bile tolerance in Listeria monocytogenes . . Infect Immun 77:, 4895–4904. [CrossRef] [PubMed]
    [Google Scholar]
  153. Welsh D. T. . ( 2000;). Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. . FEMS Microbiol Rev 24:, 263–290. [CrossRef] [PubMed]
    [Google Scholar]
  154. Wemekamp-Kamphuis H. H. , Wouters J. A. , Sleator R. D. , Gahan C. G. , Hill C. , Abee T. . ( 2002;). Multiple deletions of the osmolyte transporters BetL, Gbu, and OpuC of Listeria monocytogenes affect virulence and growth at high osmolarity. . Appl Environ Microbiol 68:, 4710–4716. [CrossRef] [PubMed]
    [Google Scholar]
  155. Wemekamp-Kamphuis H. H. , Sleator R. D. , Wouters J. A. , Hill C. , Abee T. . ( 2004;). Molecular and physiological analysis of the role of osmolyte transporters BetL, Gbu, and OpuC in growth of Listeria monocytogenes at low temperatures. . Appl Environ Microbiol 70:, 2912–2918. [CrossRef] [PubMed]
    [Google Scholar]
  156. Yamamoto K. , Hirao K. , Oshima T. , Aiba H. , Utsumi R. , Ishihama A. . ( 2005;). Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli . . J Biol Chem 280:, 1448–1456. [CrossRef] [PubMed]
    [Google Scholar]
  157. Yancey P. H. . ( 2005;). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. . J Exp Biol 208:, 2819–2830. [CrossRef] [PubMed]
    [Google Scholar]
  158. Zhang L. , Xu Z. , Patel B. K. . ( 2007;). Bacillus decisifrondis sp. nov., isolated from soil underlying decaying leaf foliage. . Int J Syst Evol Microbiol 57:, 974–978. [CrossRef] [PubMed]
    [Google Scholar]
  159. Zhu Y. , Jameson E. , Crosatti M. , Schäfer H. , Rajakumar K. , Bugg T. D. , Chen Y. . ( 2014;). Carnitine metabolism to trimethylamine by an unusual Rieske-type oxygenase from human microbiota. . Proc Natl Acad Sci U S A 111:, 4268–4273. [CrossRef] [PubMed]
    [Google Scholar]
  160. Ziegler C. , Bremer E. , Krämer R. . ( 2010;). The BCCT family of carriers: from physiology to crystal structure. . Mol Microbiol 78:, 13–34. [PubMed]
    [Google Scholar]
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