1887

Abstract

is a foodborne pathogen causing listeriosis. Acid is one of the stresses that foodborne pathogens encounter most frequently. The ability to survive and proliferate in acidic environments is a prerequisite for infection. However, there is limited knowledge about the molecular basis of adaptation of to acid. Arginine deiminase (ADI) and agmatine deiminase (AgDI) systems are implicated in bacterial tolerance to acidic environments. Homologues of ADI and AgDI systems have been found in lineages I and II strains. Sequence analysis indicated that encodes a putative carbamoyltransferase containing conserved motifs and residues important for substrate binding. Lmo0036 acted as an ornithine carbamoyltransferase and putrescine carbamoyltransferase, representing the first example, to our knowledge, that catalyses reversible ornithine and putrescine carbamoyltransfer reactions. Catabolic ornithine and putrescine carbamoyltransfer reactions constitute the second step of ADI and AgDI pathways. However, the equilibrium of carbamoyltransfer reactions was overwhelmingly towards the anabolic direction, suggesting that catabolic carbamoyltransferase was probably the limiting step of the pathways. was induced at the transcriptional level when was subjected to low-pH stress. Its expression product in exhibited higher catabolic carbamoyltransfer activities under acidic conditions. Consistently, absence of this enzyme impaired the growth of under mild acidic conditions (pH 4.8) and reduced its survival in synthetic human gastric fluid (pH 2.5), and corresponded to a loss in ammonia production, indicating that Lmo0036 was responsible for acid tolerance at both sublethal and lethal pH levels. Furthermore, Lmo0036 played a possible role in virulence.

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2011-11-01
2019-10-18
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References

  1. Arena M. E. , Manca de Nadra M. C. , Muñoz R. . ( 2002; ). The arginine deiminase pathway in the wine lactic acid bacterium Lactobacillus hilgardii X1B: structural and functional study of the arcABC genes. . Gene 301:, 61–66.[PubMed] [CrossRef]
    [Google Scholar]
  2. Bowman J. P. , Lee Chang K. J. , Pinfold T. , Ross T. . ( 2010; ). Transcriptomic and phenotypic responses of Listeria monocytogenes strains possessing different growth efficiencies under acidic conditions. . Appl Environ Microbiol 76:, 4836–4850.[PubMed] [CrossRef]
    [Google Scholar]
  3. Boyde T. R. , Rahmatullah M. . ( 1980; ). Optimization of conditions for the colorimetric determination of citrulline, using diacetyl monoxime. . Anal Biochem 107:, 424–431.[PubMed] [CrossRef]
    [Google Scholar]
  4. Byelashov O. A. , Daskalov H. , Geornaras I. , Kendall P. A. , Belk K. E. , Scanga J. A. , Smith G. C. , Sofos J. N. . ( 2010; ). Reduction of Listeria monocytogenes on frankfurters treated with lactic acid solutions of various temperatures. . Food Microbiol 27:, 783–790.[PubMed] [CrossRef]
    [Google Scholar]
  5. Casiano-Colón A. , Marquis R. E. . ( 1988; ). Role of the arginine deiminase system in protecting oral bacteria and an enzymatic basis for acid tolerance. . Appl Environ Microbiol 54:, 1318–1324.[PubMed]
    [Google Scholar]
  6. Chen J. . ( 2010; ). Listeria monocytogenes: molecular evolution and functional genomics under acidic conditions . . Hangzhou, China: PhD thesis, Zhejiang University;
  7. Chen J. , Zhang X. , Mei L. , Jiang L. , Fang W. . ( 2009a; ). Prevalence of Listeria in Chinese food products from 13 provinces between 2000 and 2007 and virulence characterization of Listeria monocytogenes isolates. . Foodborne Pathog Dis 6:, 7–14.[PubMed] [CrossRef]
    [Google Scholar]
  8. Chen J. , Luo X. , Jiang L. , Jin P. , Wei W. , Liu D. , Fang W. . ( 2009b; ). Molecular characteristics and virulence potential of Listeria monocytogenes isolates from Chinese food systems. . Food Microbiol 26:, 103–111.[PubMed] [CrossRef]
    [Google Scholar]
  9. Chen J. , Jiang L. , Chen X. , Luo X. , Chen Y. , Yu Y. , Tian G. , Liu D. , Fang W. . ( 2009c; ). Listeria monocytogenes serovar 4a is a possible evolutionary intermediate between L. monocytogenes serovars 1/2a and 4b and L. innocua . . J Microbiol Biotechnol 19:, 238–249.[PubMed]
    [Google Scholar]
  10. Chen J. , Jiang L. , Chen Q. , Zhao H. , Luo X. , Chen X. , Fang W. . ( 2009d; ). lmo0038 is involved in acid and heat stress responses and specific for Listeria monocytogenes lineages I and II, and Listeria ivanovii . . Foodborne Pathog Dis 6:, 365–376.[PubMed] [CrossRef]
    [Google Scholar]
  11. Chen J. , Chen Q. , Jiang J. , Hu H. , Ye J. , Fang W. . ( 2010a; ). Serovar 4b complex predominates among Listeria monocytogenes isolates from imported aquatic products in China. . Foodborne Pathog Dis 7:, 31–41.[PubMed] [CrossRef]
    [Google Scholar]
  12. Chen J. , Chen Q. , Jiang L. , Cheng C. , Bai F. , Wang J. , Mo F. , Fang W. . ( 2010b; ). Internalin profiling and multilocus sequence typing suggest four Listeria innocua subgroups with different evolutionary distances from Listeria monocytogenes . . BMC Microbiol 10:, 97.[PubMed] [CrossRef]
    [Google Scholar]
  13. Conte M. P. , Petrone G. , Di Biase A. M. , Ammendolia M. G. , Superti F. , Seganti L. . ( 2000; ). Acid tolerance in Listeria monocytogenes influences invasiveness of enterocyte-like cells and macrophage-like cells. . Microb Pathog 29:, 137–144.[PubMed] [CrossRef]
    [Google Scholar]
  14. Cotter P. D. , Hill C. . ( 2003; ). Surviving the acid test: responses of Gram-positive bacteria to low pH. . Microbiol Mol Biol Rev 67:, 429–453.[PubMed] [CrossRef]
    [Google Scholar]
  15. Cotter P. D. , Gahan C. G. , Hill C. . ( 2000; ). Analysis of the role of the Listeria monocytogenes F0F1-ATPase operon in the acid tolerance response. . Int J Food Microbiol 60:, 137–146.[PubMed] [CrossRef]
    [Google Scholar]
  16. Cotter P. D. , Gahan C. G. , Hill C. . ( 2001; ). A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. . Mol Microbiol 40:, 465–475.[PubMed] [CrossRef]
    [Google Scholar]
  17. Cunin R. , Glansdorff N. , Piérard A. , Stalon V. . ( 1986; ). Biosynthesis and metabolism of arginine in bacteria. . Microbiol Rev 50:, 314–352.[PubMed]
    [Google Scholar]
  18. de Chastellier C. , Berche P. . ( 1994; ). Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria. . Infect Immun 62:, 543–553.[PubMed]
    [Google Scholar]
  19. De la Fuente J. L. , Martin J. F. , Liras P. . ( 1996; ). New type of hexameric ornithine carbamoyltransferase with arginase activity in the cephamycin producers Streptomyces clavuligerus and Nocardia lactamdurans . . Biochem J 320:, 173–179.[PubMed]
    [Google Scholar]
  20. Degnan B. A. , Fontaine M. C. , Doebereiner A. H. , Lee J. J. , Mastroeni P. , Dougan G. , Goodacre J. A. , Kehoe M. A. . ( 2000; ). Characterization of an isogenic mutant of Streptococcus pyogenes Manfredo lacking the ability to make streptococcal acid glycoprotein. . Infect Immun 68:, 2441–2448.[PubMed] [CrossRef]
    [Google Scholar]
  21. Freitag N. E. , Port G. C. , Miner M. D. . ( 2009; ). Listeria monocytogenes – from saprophyte to intracellular pathogen. . Nat Rev Microbiol 7:, 623–628.[PubMed] [CrossRef]
    [Google Scholar]
  22. Fulde M. , Willenborg J. , de Greeff A. , Benga L. , Smith H. E. , Valentin-Weigand P. , Goethe R. . ( 2011; ). ArgR is an essential local transcriptional regulator of the arcABC operon in Streptococcus suis and is crucial for biological fitness in an acidic environment. . Microbiology 157:, 572–582.[PubMed] [CrossRef]
    [Google Scholar]
  23. Glaser P. , Frangeul L. , Buchrieser C. , Rusniok C. , Amend A. , Baquero F. , Berche P. , Bloecker H. , Brandt P. et al. ( 2001; ). Comparative genomics of Listeria species. . Science 294:, 849–852.[PubMed]
    [Google Scholar]
  24. Griswold A. R. , Chen Y. Y. M. , Burne R. A. . ( 2004; ). Analysis of an agmatine deiminase gene cluster in Streptococcus mutans UA159. . J Bacteriol 186:, 1902–1904.[PubMed] [CrossRef]
    [Google Scholar]
  25. Gruening P. , Fulde M. , Valentin-Weigand P. , Goethe R. . ( 2006; ). Structure, regulation, and putative function of the arginine deiminase system of Streptococcus suis . . J Bacteriol 188:, 361–369.[PubMed] [CrossRef]
    [Google Scholar]
  26. Jiang J. , Chen J. , Cheng C. , Hu H. , Bai F. , Chen N. , Yan G. , Fang W. . ( 2011; ). Disruption of InlC2 enhances the internalization of Listeria monocytogenes by epithelial cells. . World J Microbiol Biotechnol 27:, 2155–2161.[CrossRef]
    [Google Scholar]
  27. Joseph B. , Przybilla K. , Stühler C. , Schauer K. , Slaghuis J. , Fuchs T. M. , Goebel W. . ( 2006; ). Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. . J Bacteriol 188:, 556–568.[PubMed] [CrossRef]
    [Google Scholar]
  28. Landete J. M. , Arena M. E. , Pardo I. , Manca de Nadra M. C. , Ferrer S. . ( 2008; ). Comparative survey of putrescine production from agmatine deamination in different bacteria. . Food Microbiol 25:, 882–887.[PubMed] [CrossRef]
    [Google Scholar]
  29. Legrain C. , Stalon V. . ( 1976; ). Ornithine carbamoyltransferase from Escherichia coli W. Purification, structure and steady-state kinetic analysis. . Eur J Biochem 63:, 289–301.[PubMed] [CrossRef]
    [Google Scholar]
  30. Legrain C. , Stalon V. , Noullez J. P. , Mercenier A. , Simon J. P. , Broman K. , Wiame J. M. . ( 1977; ). Structure and function of ornithine carbamoyltransferases. . Eur J Biochem 80:, 401–409.[PubMed] [CrossRef]
    [Google Scholar]
  31. Liu D. . ( 2006; ). Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. . J Med Microbiol 55:, 645–659.[PubMed] [CrossRef]
    [Google Scholar]
  32. Llácer J. L. , Polo L. M. , Tavárez S. , Alarcón B. , Hilario R. , Rubio V. . ( 2007; ). The gene cluster for agmatine catabolism of Enterococcus faecalis: study of recombinant putrescine transcarbamylase and agmatine deiminase and a snapshot of agmatine deiminase catalyzing its reaction. . J Bacteriol 189:, 1254–1265.[PubMed] [CrossRef]
    [Google Scholar]
  33. Lucas P. M. , Blancato V. S. , Claisse O. , Magni C. , Lolkema J. S. , Lonvaud-Funel A. . ( 2007; ). Agmatine deiminase pathway genes in Lactobacillus brevis are linked to the tyrosine decarboxylation operon in a putative acid resistance locus. . Microbiology 153:, 2221–2230.[PubMed] [CrossRef]
    [Google Scholar]
  34. Marquis R. E. , Bender G. R. , Murray D. R. , Wong A. . ( 1987; ). Arginine deiminase system and bacterial adaptation to acid environments. . Appl Environ Microbiol 53:, 198–200.[PubMed]
    [Google Scholar]
  35. Marron L. , Emerson N. , Gahan C. G. , Hill C. . ( 1997; ). A mutant of Listeria monocytogenes LO28 unable to induce an acid tolerance response displays diminished virulence in a murine model. . Appl Environ Microbiol 63:, 4945–4947.[PubMed]
    [Google Scholar]
  36. Milillo S. R. , Badamo J. M. , Wiedmann M. . ( 2009; ). Contributions to selected phenotypic characteristics of large species- and lineage-specific genomic regions in Listeria monocytogenes . . Food Microbiol 26:, 212–223.[PubMed] [CrossRef]
    [Google Scholar]
  37. Naumoff D. G. , Xu Y. , Glansdorff N. , Labedan B. . ( 2004; ). Retrieving sequences of enzymes experimentally characterized but erroneously annotated: the case of the putrescine carbamoyltransferase. . BMC Genomics 5:, 52.[PubMed] [CrossRef]
    [Google Scholar]
  38. O’Driscoll B. , Gahan C. G. , Hill C. . ( 1996; ). Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. . Appl Environ Microbiol 62:, 1693–1698.[PubMed]
    [Google Scholar]
  39. Orsi R. H. , den Bakker H. C. , Wiedmann M. . ( 2011; ). Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. . Int J Med Microbiol 301:, 79–96.[PubMed] [CrossRef]
    [Google Scholar]
  40. Ramón-Maiques S. , Marina A. , Guinot A. , Gil-Ortiz F. , Uriarte M. , Fita I. , Rubio V. . ( 2010; ). Substrate binding and catalysis in carbamate kinase ascertained by crystallographic and site-directed mutagenesis studies: movements and significance of a unique globular subdomain of this key enzyme for fermentative ATP production in bacteria. . J Mol Biol 397:, 1261–1275.[PubMed] [CrossRef]
    [Google Scholar]
  41. Ren Y. , Zhang Y. , Shao S. , Cai Z. , Feng L. , Pan H. , Wang Z. . ( 2007; ). Simultaneous determination of multi-component mycotoxin contaminants in foods and feeds by ultra-performance liquid chromatography tandem mass spectrometry. . J Chromatogr A 1143:, 48–64.[PubMed] [CrossRef]
    [Google Scholar]
  42. Ryan S. , Begley M. , Gahan C. G. M. , Hill C. . ( 2009; ). Molecular characterization of the arginine deiminase system in Listeria monocytogenes: regulation and role in acid tolerance. . Environ Microbiol 11:, 432–445.[PubMed] [CrossRef]
    [Google Scholar]
  43. Sainz G. , Tricot C. , Foray M. F. , Marion D. , Dideberg O. , Stalon V. . ( 1998; ). Kinetic studies of allosteric catabolic ornithine carbamoyltransferase from Pseudomonas aeruginosa . . Eur J Biochem 251:, 528–533.[PubMed] [CrossRef]
    [Google Scholar]
  44. Sleator R. D. , Watson D. , Hill C. , Gahan C. G. . ( 2009; ). The interaction between Listeria monocytogenes and the host gastrointestinal tract. . Microbiology 155:, 2463–2475.[PubMed] [CrossRef]
    [Google Scholar]
  45. Swaminathan B. , Gerner-Smidt P. . ( 2007; ). The epidemiology of human listeriosis. . Microbes Infect 9:, 1236–1243.[PubMed] [CrossRef]
    [Google Scholar]
  46. Vrancken G. , Rimaux T. , Wouters D. , Leroy F. , De Vuyst L. . ( 2009a; ). The arginine deiminase pathway of Lactobacillus fermentum IMDO 130101 responds to growth under stress conditions of both temperature and salt. . Food Microbiol 26:, 720–727.[PubMed] [CrossRef]
    [Google Scholar]
  47. Vrancken G. , Rimaux T. , Weckx S. , De Vuyst L. , Leroy F. . ( 2009b; ). Environmental pH determines citrulline and ornithine release through the arginine deiminase pathway in Lactobacillus fermentum IMDO 130101. . Int J Food Microbiol 135:, 216–222.[PubMed] [CrossRef]
    [Google Scholar]
  48. Ward T. J. , Ducey T. F. , Usgaard T. , Dunn K. A. , Bielawski J. P. . ( 2008; ). Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. . Appl Environ Microbiol 74:, 7629–7642.[PubMed] [CrossRef]
    [Google Scholar]
  49. Wargnies B. , Lauwers N. , Stalon V. . ( 1979; ). Structure and properties of the putrescine carbamoyltransferase of Streptococcus faecalis . . Eur J Biochem 101:, 143–152.[PubMed] [CrossRef]
    [Google Scholar]
  50. Wu B. , Xia C. , Du X. , Cao X. , Shen J. . ( 2006; ). Influence of anti-FloR antibody on florfenicol accumulation in florfenicol-resistant Escherichia coli and enzyme-linked immunosorbent assay for detection of florfenicol-resistant E. coli isolates. . J Clin Microbiol 44:, 378–382.[PubMed] [CrossRef]
    [Google Scholar]
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