1887

Abstract

Manganese serves an important function in in protection against oxidative stress and this bacterium can accumulate Mn up to millimolar levels intracellularly. Although the physiological role of Mn and the uptake of this metal ion have been well documented, the only uptake system described so far for this bacterium is the Mn- and Cd-specific P-type ATPase (MntA). Recently, the genome of WCFS1 has been sequenced allowing detection of genes potentially encoding Mn transport systems, using established microbial Mn transporters as the query sequence. This genome analysis revealed that WCFS1 encodes, besides the previously described gene, an ABC transport system () and three genes encoding Nramp transporters (, and ). The expression of three (, and ) of the five transport systems was specifically derepressed or induced upon Mn limitation, supporting their role in Mn homeostasis in . However, in contrast to previous reports, expression remains below detection levels in both Northern and real-time RT-PCR analysis in both Mn excess and starvation conditions. Growth of WCFS1 derivatives mutated in , or , or both and appears unaffected under Mn excess or Mn limitation. Moreover, intracellular Mn concentrations remained unaltered in these mutants compared to the wild-type. This may suggest that this species is highly adaptive in response to inactivation of these genes or, alternatively, that other transporters that have not yet been identified as Mn transporters in bacteria are involved in Mn homeostasis in .

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2005-04-01
2019-10-15
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References

  1. Archibald, F. S. & Duong, M.-N. ( 1984; ). Manganese acquisition by Lactobacillus plantarum. J Bacteriol 158, 1–8.
    [Google Scholar]
  2. Archibald, F. S. & Fridovich, I. ( 1981a; ). Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J Bacteriol 146, 928–936.
    [Google Scholar]
  3. Archibald, F. S. & Fridovich, I. ( 1981b; ). Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J Bacteriol 145, 442–451.
    [Google Scholar]
  4. Aukrust, T. & Blom, H. ( 1992; ). Transformation of Lactobacillus strains used in meat and vegetable fermentations. Food Res Int 25, 253–261.[CrossRef]
    [Google Scholar]
  5. Axelsen, K. & Palmgren, M. G. ( 1998; ). Evolution of substrate specificity in the P-type ATPase superfamily. J Mol Evol 46, 84–101.[CrossRef]
    [Google Scholar]
  6. Bartsevich, V. V. & Pakrasi, H. B. ( 1995; ). Molecular identification of an ABC transporter complex for manganese: analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process. EMBO J 14, 1845–1853.
    [Google Scholar]
  7. Bearden, S. W. & Perry, R. D. ( 1999; ). The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plaque. Mol Microbiol 32, 403–414.[CrossRef]
    [Google Scholar]
  8. Bolotin, A., Wincker, P., Mauger, S., Jaillon, O., Malarme, K., Weissenbach, J., Ehrlich, S. D. & Sorokin, A. ( 2001; ). The complete genome sequence of the lactic acid bacterium Lactococcus lactis IL1403. Genome Res 11, 731–753.[CrossRef]
    [Google Scholar]
  9. Bradford, M. M. ( 1976; ). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254.[CrossRef]
    [Google Scholar]
  10. Claverys, J.-P. ( 2001; ). A new family of high-affinity ABC manganese and zinc permeases. Res Microbiol 152, 231–243.[CrossRef]
    [Google Scholar]
  11. Daly, M. J., Gaidamakova, E. K. & 11 other authors ( 2004; ). Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306, 1025–1028.[CrossRef]
    [Google Scholar]
  12. Dintilhac, A., Alloing, G., Granadel, C. & Claverys, J.-P. ( 1997; ). Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol 25, 727–739.[CrossRef]
    [Google Scholar]
  13. Ferretti, J. J., McShan, W. M., Ajdic, D. & 20 other authors ( 2001; ). Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci U S A 10, 4658–4663.
    [Google Scholar]
  14. Forbes, J. R. & Gros, P. ( 2001; ). Divalent-metal transport by NRAMP proteins at the interface of host–pathogen interactions. Trends Microbiol 9, 397–403.[CrossRef]
    [Google Scholar]
  15. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557–580.[CrossRef]
    [Google Scholar]
  16. Hao, Z., Chen, S. & Wilson, D. B. ( 1999a; ). Cloning, expression, and characterization of cadmium and manganese uptake genes from Lactobacillus plantarum. Appl Environ Microbiol 65, 4746–4752.
    [Google Scholar]
  17. Hao, Z., Reiske, H. R. & Wilson, D. B. ( 1999b; ). Characterization of cadmium uptake in Lactobacillus plantarum and isolation of cadmium and manganese uptake mutants. Appl Environ Microbiol 65, 4741–4745.
    [Google Scholar]
  18. Hastings, J. W., Holzapfel, W. H. & Niemand, J. G. ( 1986; ). Radiation resistance of lactobacilli isolated from radurized meat relative to growth and environment. Appl Environ Microbiol 52, 898–901.
    [Google Scholar]
  19. Hayashi, N., Ito, M., Horiike, S. & Taguchi, H. ( 2001; ). Molecular cloning of a putative divalent-cation transporter gene as a new genetic marker for the identification of Lactobacillus brevis strains capable of growing in beer. Appl Microbiol Biotechnol 55, 596–603.[CrossRef]
    [Google Scholar]
  20. Jakubovics, N. S., Smith, A. W. & Jenkinson, H. F. ( 2000; ). Expression of the virulence-related Sca (Mn2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol Microbiol 38, 140–153.[CrossRef]
    [Google Scholar]
  21. Jakubovics, N. S., Smith, A. W. & Jenkinson, H. F. ( 2002; ). Oxidative stress tolerance is manganese (Mn2+) regulated in Streptococcus gordonii. Microbiology 148, 3255–3263.
    [Google Scholar]
  22. Janulczyk, R., Ricci, S. & Björck, L. ( 2003; ). MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes. Infect Immun 71, 2656–2664.[CrossRef]
    [Google Scholar]
  23. Kehres, D. G. & Maguire, M. E. ( 2003; ). Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 27, 263–290.[CrossRef]
    [Google Scholar]
  24. Kehres, D., Zaharik, M. L., Brett Finlay, B. & Maquire, M. E. ( 2000; ). The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36, 1085–1100.[CrossRef]
    [Google Scholar]
  25. Kehres, D. G., Janakiraman, A., Slauch, J. M. & Maguire, M. E. ( 2002; ). SitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar Typhimurium. J Bacteriol 184, 3159–3166.[CrossRef]
    [Google Scholar]
  26. 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]
  27. Kleerebezem, M., Boekhorst, J., Van Kranenburg, R. & 17 other authors ( 2003; ). Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100, 1990–1995.[CrossRef]
    [Google Scholar]
  28. Kolenbrander, P. E., Andersen, R. N., Baker, R. A. & Jenkinson, H. F. ( 1998; ). The adhesin-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol 180, 290–295.
    [Google Scholar]
  29. Kuipers, O. P., Beerthuyzen, M. M., Siezen, R. J. & de Vos, W. M. ( 1993; ). Characterization of the nisin gene cluster nisABTCIPR of Lactococcus lactis. Requirements of expression of the nisA and nisI genes for the development of immunity. Eur J Biochem 216, 281–291.[CrossRef]
    [Google Scholar]
  30. Lawrence, M. C., Pilling, P. A., Epa, V. C., Berry, A. M., Ogunniyi, A. D. & Paton, J. C. ( 1998; ). The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 6, 1553–1561.[CrossRef]
    [Google Scholar]
  31. Maeda, T., Sugiura, R., Kita, A. & 8 other authors ( 2004; ). Pmr1, a P-type ATPase, and Pdt1, an Nramp homologue, cooperatively regulate cell morphogenesis in fission yeast: the importance of Mn2+ homeostasis. Genes Cells 9, 71–82.[CrossRef]
    [Google Scholar]
  32. Makui, H., Roig, E., Cole, S. T., Helmann, J. D., Gros, P. & Cellier, M. F. M. ( 2000; ). Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol 35, 1065–1078.[CrossRef]
    [Google Scholar]
  33. Nielsen, H., Engelbrecht, J., Brunak, S. & von Heijne, G. ( 1997; ). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Prot Eng 10, 1–6.[CrossRef]
    [Google Scholar]
  34. Nierop Groot, M. N. & de Bont, J. A. M. ( 1998; ). Conversion of phenylalanine to benzaldehyde initiated by an aminotransferase in Lactobacillus plantarum. Appl Environ Microbiol 64, 3009–3013.
    [Google Scholar]
  35. Nierop Groot, M. N. & de Bont, J. A. M. ( 1999; ). Involvement of manganese in conversion of phenylalanine to benzaldehyde by lactic acid bacteria. Appl Environ Microbiol 65, 5590–5593.
    [Google Scholar]
  36. Paik, S., Brown, A., Munro, C. L., Cornelissen, C. N. & Kitten, T. ( 2003; ). The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J Bacteriol 185, 5967–5975.[CrossRef]
    [Google Scholar]
  37. Pfaffl, M. W. ( 2001; ). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, 2003–2007.[CrossRef]
    [Google Scholar]
  38. Pfaffl, M. W., Horgan, G. W. & Dempfle, L. ( 2002; ). Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30, E36.[CrossRef]
    [Google Scholar]
  39. Que, Q. & Helmann, J. D. ( 2000; ). Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphteria toxin repressor family of proteins. Mol Microbiol 35, 1454–1468.
    [Google Scholar]
  40. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.
  41. Sampson, J. S., O'Connor, S. P., Stinson, A. R., Tharpe, J. A. & Russel, H. ( 1994; ). Cloning and nucleotide sequence analysis of psaA, the Streptococcus pneumoniae gene encoding a 37-kilodalton protein homologous to previously reported Streptococcus sp. adhesins. Infect Immun 62, 319–324.
    [Google Scholar]
  42. Simpson, W. J. ( 1993; ). Ionophoric action of trans-isohumulone on Lactobacillus brevis. J Gen Microbiol 139, 1041–1045.[CrossRef]
    [Google Scholar]
  43. Sutcliffe, I. C. & Russel, R. R. B. ( 1995; ). Lipoproteins of Gram-positive bacteria. Minireview. J Bacteriol 177, 1123–1128.
    [Google Scholar]
  44. Tettelin, H., Nelson, K. E., Paulsen, I. T. & 36 other authors ( 2001; ). Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293, 498–506.[CrossRef]
    [Google Scholar]
  45. Ton, V.-K., Mandal, D., Vahadji, C. & Rao, R. ( 2002; ). Functional expression in yeast of the human secretory pathway Ca2+, Mn2+-ATPase defective in Hailey–Hailey disease. J Biol Chem 22, 6422–6427.
    [Google Scholar]
  46. Van Kranenburg, R., Marugg, J. D., Van Swam, I. I., Willem, N. J. & de Vos, W. M. ( 1997; ). Molecular characterization of the plasmid-encoded eps gene cluster essential for exopolysaccharide biosynthesis in Lactococcus lactis. Mol Microbiol 24, 387–397.[CrossRef]
    [Google Scholar]
  47. Van Rooijen, R. J. & de Vos, W. M. ( 1990; ). Molecular cloning, transcriptional analysis, and nucleotide sequence of lacR, a gene encoding the repressor of the lactose phosphotransferase system of Lactococcus lactis. J Biol Chem 265, 18499–18503.
    [Google Scholar]
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