Skip to main content
Log in

MgtC as a Horizontally-Acquired Virulence Factor of Intracellular Bacterial Pathogens: Evidence from Molecular Phylogeny and Comparative Genomics

  • Letter to the Editor
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

MgtC is a virulence factor required for intramacrophage survival and growth in low Mg2+ medium in two pathogens that are not phylogenetically related, Salmonella typhimurium and Mycobacterium tuberculosis. In S. typhimurium, mgtC is carried by the SPI-3 pathogenicity island and hybridization studies have suggested that the distribution of mgtC among enterobacteria is limited. In the present study, we searched for the presence of mgtC-like sequences in eubacterial genomes. Analyses of MgtC-like proteins phylogeny and mgtC-like chromosomal context support the hypothesis that mgtC has been acquired by horizontal gene transfer repeatedly throughout bacterial evolution. In addition, the phylogenetic analysis revealed the existence of a subgroup of proteins, that includes the S. typhimurium and M. tuberculosis MgtC proteins, as well as MgtC-related proteins from other pathogens that are able to survive in macrophages, B. melitensis and Y. pestis. We propose that MgtC has a similar function in all these distantly related pathogens, most likely providing the ability to grow in a low Mg2+ environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

References

  1. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694

    PubMed  Google Scholar 

  2. A-B Blanc-Potard EA Groisman (1997) ArticleTitleThe Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16 5376–5385 Occurrence Handle10.1093/emboj/16.17.5376 Occurrence Handle1:CAS:528:DyaK2sXmsVGlsL0%3D Occurrence Handle9311997

    Article  CAS  PubMed  Google Scholar 

  3. A-B Blanc-Potard F Solomon J Kayser EA Groisman (1999) ArticleTitleThe SPI-3 pathogenicity island of Salmonella enterica. J Bacteriol 181 998–1004 Occurrence Handle1:CAS:528:DyaK1MXhtVGis74%3D Occurrence Handle9922266

    CAS  PubMed  Google Scholar 

  4. ML Boschiroli V Foulongne D O’Callaghan (2001) ArticleTitleBrucellosis: A worldwide zoonosis. Curr Opin Microbiol 4 58–64 Occurrence Handle10.1016/S1369-5274(00)00165-X Occurrence Handle1:STN:280:DC%2BD3M3jt1yqtg%3D%3D Occurrence Handle11173035

    Article  CAS  PubMed  Google Scholar 

  5. N Buchmeier A-B Blanc-Potard S Ehrt D Piddington L Riley EA Groisman (2000) ArticleTitleA parallel intraphagosomal survival strategy shared by Mycobacterium tuberculosis and Salmonella enterica. Mol Microbiol 35 1375–1382 Occurrence Handle10.1046/j.1365-2958.2000.01797.x Occurrence Handle1:CAS:528:DC%2BD3cXis1Wrtr8%3D Occurrence Handle10760138

    Article  CAS  PubMed  Google Scholar 

  6. S Eriksson S Lucchini A Thompson M Rhen JC Hinton (2003) ArticleTitleUnravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Microbiol 47 103–118 Occurrence Handle10.1046/j.1365-2958.2003.03313.x Occurrence Handle1:CAS:528:DC%2BD3sXntVKiuw%3D%3D

    Article  CAS  Google Scholar 

  7. Felsenstein J (2002) Phylip (Phylip inference package), version 3.6(alpha3). http://evolution.genetics.washington.edu/phylip/phylip36.html

  8. N Galtier M Gouy C Gautier (1996) ArticleTitleSeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny. Comput Applic Biosci 12 543–548 Occurrence Handle1:CAS:528:DyaK2sXhtlWktLw%3D

    CAS  Google Scholar 

  9. T Guina SO Purvine EC Yi J Eng DR Goodlett R Aebersold SI Miller (2003) ArticleTitleQuantitative proteomic analysis indicates increased synthesis of a quinolone by Pseudomonas aeruginosa isolates from cystic fibrosis airways. Proc Natl Acad Sci USA 100 2771–2776 Occurrence Handle10.1073/pnas.0435846100 Occurrence Handle1:CAS:528:DC%2BD3sXitVait7c%3D Occurrence Handle12601166

    Article  CAS  PubMed  Google Scholar 

  10. YM Hou (1999) ArticleTitleTransfer RNAs and pathogenicity islands. Trends Biochem Sci 24 295–298 Occurrence Handle10.1016/S0968-0004(99)01428-0 Occurrence Handle1:CAS:528:DC%2BD3cXjtVKruw%3D%3D Occurrence Handle10431171

    Article  CAS  PubMed  Google Scholar 

  11. DT Jones WR Taylor JM Thornton (1992) ArticleTitleThe rapid generation of mutation data matrices from protein sequences. Comput Applic Biosci 8 275–282 Occurrence Handle1:CAS:528:DyaK38Xlt1Okt7w%3D

    CAS  Google Scholar 

  12. DG Kehres ME Maguire (2002) ArticleTitleStructure, properties and regulation of magnesium transport proteins. Biometals 15 261–270 Occurrence Handle10.1023/A:1016078832697 Occurrence Handle1:CAS:528:DC%2BD38XkvFCgtLY%3D Occurrence Handle12206392

    Article  CAS  PubMed  Google Scholar 

  13. JG Lawrence H Ochman (2002) ArticleTitleReconciling the many faces of lateral gene transfer. Trends Microbiol 10 1–4 Occurrence Handle10.1016/S0966-842X(01)02282-X Occurrence Handle1:CAS:528:DC%2BD38Xntlaguw%3D%3D Occurrence Handle11755071

    Article  CAS  PubMed  Google Scholar 

  14. JG Lawrence H Ochman (1997) ArticleTitleAmelioration of bacterial genomes: Rates of change and exchange. J Mol Evol 44 383–397 Occurrence Handle1:CAS:528:DyaK2sXis12msLw%3D Occurrence Handle9089078

    CAS  PubMed  Google Scholar 

  15. P Lestrate RM Delrue I Danese C Didembourg B Taminiau P Mertens et al. (2000) ArticleTitleIdentification and characterization of in vivo attenuated mutants of Brucella melitensis. Mol Microbiol 38 543–551 Occurrence Handle10.1046/j.1365-2958.2000.02150.x Occurrence Handle1:CAS:528:DC%2BD3cXovV2isrc%3D Occurrence Handle11069678

    Article  CAS  PubMed  Google Scholar 

  16. PC Oyston N Dorrell K Williams SR Li M Green RW Titball BW Wren (2000) ArticleTitleThe response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 68 3419–3425 Occurrence Handle10.1128/IAI.68.6.3419-3425.2000 Occurrence Handle1:CAS:528:DC%2BD3cXjsF2js7w%3D Occurrence Handle10816493

    Article  CAS  PubMed  Google Scholar 

  17. G Perrière M Gouy (1996) ArticleTitleWWW-Query: An on-line retrieval system for biological sequence banks. Biochimie 78 364–369 Occurrence Handle8905155

    PubMed  Google Scholar 

  18. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2000) TREE-PUZZLE version 5.0. Maximum likelihood analysis for nucleotide, amino acid, and two-state data, http://www.tree-puzzle.de/

  19. RL Smith MT Kaczmarek LM Kucharski ME Maguire (1998) ArticleTitleMagnesium transport in Salmonella typhimurium: Regulation of mgtA and mgtCB during invasion of epithelial and macrophage cells. Microbiology 144 1835–1843 Occurrence Handle1:CAS:528:DyaK1cXltVyhs7o%3D Occurrence Handle9695916

    CAS  PubMed  Google Scholar 

  20. MD Snavely CG Miller ME Maguire (1991) ArticleTitleThe mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 266 815–823 Occurrence Handle1:CAS:528:DyaK3MXkt1ehtbg%3D Occurrence Handle1824701

    CAS  PubMed  Google Scholar 

  21. SC Straley PA Harmon (1984) ArticleTitle Yersinia pestis grows within phagolysosomes in mouse peritoneal macrophages. Infect Immun 45 655–659 Occurrence Handle1:STN:280:BiuB1cjotlM%3D Occurrence Handle6469352

    CAS  PubMed  Google Scholar 

  22. DL Swofford (1998) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4.Ob10 for Macintosh PPC. Sinauer Associates Sunderland, Massachusetts

    Google Scholar 

  23. JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673–4680 Occurrence Handle7984417

    PubMed  Google Scholar 

  24. J Wei JL Dahl JW Moulder EA Roberts P O’Gaora DB Young RL Friedman (2000) ArticleTitleIdentification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages. J Bacteriol 182 377–384 Occurrence Handle10.1128/JB.182.2.377-384.2000 Occurrence Handle1:CAS:528:DC%2BD3cXivFSgug%3D%3D Occurrence Handle10629183

    Article  CAS  PubMed  Google Scholar 

  25. YI Wolf IB Rogozin AS Kondrashov EV Koonin (2001) ArticleTitleGenome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. Genome Res 11 356–372 Occurrence Handle10.1101/gr.GR-1619R Occurrence Handle1:CAS:528:DC%2BD3MXhvVOnsbg%3D Occurrence Handle11230160

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank M. Tibayrenc (director of the UMR CNRS-IRD 9926, Montpellier) for his support, E.A. Groisman (Washington University, St. Louis, Missouri), and D. O’Callaghan (Inserm U431, Nîmes, France) for critical reading of the manuscript and two anonymous reviewers for comments on a previous version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne-Béatrice Blanc-Potard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blanc-Potard, AB., Lafay, B. MgtC as a Horizontally-Acquired Virulence Factor of Intracellular Bacterial Pathogens: Evidence from Molecular Phylogeny and Comparative Genomics . J Mol Evol 57, 479–486 (2003). https://doi.org/10.1007/s00239-003-2496-4

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-2496-4

Keywords

Navigation