Skip to main content
Log in

Evidence for phylogenetic inheritance in pathogenicity of Mycobacterium

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

In this study, we attempt to highlight part of the adaptive and phylogenetic constraints in mycobacterial pathogenicity. For this purpose, we first provide a phylogeny of Mycobacteria based on cladistic analyses of 64 different taxa. We then performed a comparative analysis, taking into account both ecological factors and phylogenetic relationships. The GLIM modelling analysis showed that different ecological and phylogenetic factors might be invoked to explain the variation in pathogenicity levels. Interestingly, the most harmful species were shown to be connected with the most diversified habitats. However, the independent contrast analysis revealed that once phylogeny was taken into account, none of the relationships between ecological factors and pathogenicity remained significant, and the pathogenicity appeared to be phylogenetically inherited among mycobacteria. The most pathogen were found in the slow-growing/long helix 18 group, and within this group in the most derived taxa.

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.

Similar content being viewed by others

References

  • Agnew P. and Koella J.C. 1997. Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proc. Roy. Soc. Lond.B 264: 9–15.

    Article  CAS  Google Scholar 

  • Barriel V. 1994. Phylogénies moléculaires et insertions-délétions de nucléotides. C.R.A.S. Paris, Sciences Vie/Life Sciences 317: 693–701.

    Google Scholar 

  • Bidochka M.J., St. Leger R.J., Stuart A. and Gowanlock K. 1999. Nuclear rDNA phylogeny in the fungal genus Verticillium and its relationship to insect and plant virulence, extracellular proteases and carboxilases. Microbiol. 145: 955–963.

    CAS  Google Scholar 

  • Bowman B.H. and Taylor J.W. 1993. Molecular phylogeny of pathogenic and non pathogenic originals. In: Reynolds D.R. and Taylor J.W. (eds), The fungal Holomorph: Mitotic, Meiotic and Pleomorphic speciation in fungal systematics. CAB international, Wallingford, pp. 169–178.

    Google Scholar 

  • Bowman B.H., White T.J. and Taylor J.W. 1996. Human pathogenic fungi and their close nonpathogenic relatives. Mol. Phyl. Evol. 6: 89–96.

    Article  CAS  Google Scholar 

  • Brown B.A., Springer B., Steingrube V.A., Wilson R.W., Pfyffer G.E., Garcia M.J. et al. 1999. Mycobacterium wolinskyi sp. nov. and Mycobacterium goodii sp. nov. Two rapidly growing species related to Mycobacterium smegmatis and associated with human wound infections: a cooperative study from the International Working Group on Mycobacterial Taxonomy. Int. J. Syst. Bacteriol. 49: 1493–1511.

    PubMed  CAS  Google Scholar 

  • Collins C.H., Grange J.M. and Yates M.D. 1984. Mycobacteria in water. J. Applied Bacteriol. 57: 193–211.

    CAS  Google Scholar 

  • Ebert D. 1994. Virulence and local adaptation of a horizontally transmitted parasite. Science 265: 1084–1086.

    PubMed  Google Scholar 

  • Ebert D. and Herre E.A. 1996. The evolution of parasitic diseases. Parasitol. Today 12: 96–101.

    Article  PubMed  CAS  Google Scholar 

  • Ewald P.W. 1983. Host-parasite relations, vectors, and the evolution of disease severity. An. Rev. Ecol. Syst. 14: 465–485.

    Article  Google Scholar 

  • Ewald P.W. 1994. Evolution of Infectious Disease. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Falkinham J.O. III 1996. Epidemiology of infection by non tuberculosous mycobacteria. Clin. Microbiol. Rev. 9: 177–215.

    PubMed  Google Scholar 

  • Falkinham J.O. III 1998. Transmission of Mycobacteria. In: Gangadharam P.R.J. and Jenkins P.A. (eds), Mycobacteria I Basic Aspects. International Thomson Publishing, pp. 178–209.

  • Felsenstein J. 1985. Phylogenies and the comparative method. Am. Nat. 125: 1–15.

    Article  Google Scholar 

  • Floyd M.M., Guthertz L.S., Silcox V.A., Duffey P.S., Jang Y., Desmond E.P. et al. 1996. Characterization of an SAV organism and proposal of Mycobacterium triplex sp. nov. J. Clin. Microbiol. 34: 2963–2967.

    PubMed  CAS  Google Scholar 

  • Garland T. Jr 1992. Rate tests for phenotypic evolution using phylogenetically independent contrasts. Am. Nat. 140: 509–519.

    Article  PubMed  Google Scholar 

  • Garland T. Jr, Harvey P.H. and Ives A.R. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrast. Syst. Biol. 41: 18–32.

    Google Scholar 

  • Goodfellow M. and Magee J.G. 1998. Taxonomy of mycobacteria. In: Gangadharam P.R.J. and Jenkins P.A. (eds), Mycobacteria I Basic Aspects. International Thomson Publishing, pp. 1–71.

  • Grange J.M. 1999. Pathogenesis of mycobacterial disease. In: Gangadharam P.R.J. and Jenkins P.A. (eds), Mycobacteria I Basic Aspects. International Thomson Publishing, pp. 145–177.

  • Grosset J., Truffot-Pernot Ch., Boisvert H. and Lalande V. 1991. Qu'est ce que les mycobactéries atypiques? Méd. Mal. Infect 21 Sp.: 7–15.

    Article  Google Scholar 

  • Guégan J.F. and Morand S. 1996. Polyploid hosts: strange attractors for parasites? Oikos 77: 366–370.

    Google Scholar 

  • Haas W.H., Butler W.R., Kirschner P., Plikaytis B.B., Coyle M.B., Amthor B. et al. 1997. A new agent of mycobacterial lymphadenitis in children: Mycobacterium heidelbergense sp. nov. J. Clin. Microbiol. 35: 3203–3209.

    PubMed  CAS  Google Scholar 

  • Hamilton A.J. and Holdom M.D. 1999. Antioxidant systems in the pathogenic fungi of man and their role in virulence. Med. Mycol. 37: 375–389.

    Article  PubMed  CAS  Google Scholar 

  • Harvey P.H. and Pagel M.D. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Johnson P.D.R., Stinear T.P. and Hayman J.A. 1999. Mycobacterium ulcerans-a mini review. J. Med. Microbiol. 48: 511–513.

    Article  PubMed  CAS  Google Scholar 

  • Kuhnert P., Boerlin P. and Frey J. 2000. Target genes for virulence assessment of Escherichia coli isolates from water, food and the environment. FEMS Microbiol. Rev. 24: 107–117.

    Article  PubMed  CAS  Google Scholar 

  • Legrand E., Sola C. and Rastogi N. 2000. Le complexe Mycobacterium avium-intracellulare: marqueurs phéenotypiques et génotypiques et les bases moléculaires de la transmission interespèces. Bull. Soc. Pathol. Exot. 93: 182–192.

    PubMed  CAS  Google Scholar 

  • Lipsitch M. and Moxon E.R. 1997. Virulence and transmissibility of pathogens: what is the relationship? Trends in Microbiol. 5: 31–37.

    Article  CAS  Google Scholar 

  • Martins E.P. 1996. Phylogenies and the Comparative Method in Animal Behavior. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Maynard Smith J., Feil E.J. and Sith N.H. 2000. Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 22: 115–1122.

    Google Scholar 

  • McCullagh P. and Nelder J.A. 1989. Generalized Linear Models. 2nd edn. Chapman & Hall Ltd., London, UK.

    Google Scholar 

  • Pagel M.D. 1992. A method for the analysis of comparative data. J. Theor. Biol. 156: 431–442.

    Article  Google Scholar 

  • Philippe H. 1993. MUST: a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res. 21: 5264–5272.

    PubMed  CAS  Google Scholar 

  • Picard B., Garcia J.S., Gouriou S., Duriez P., Brahimi N., Bingen E. et al. 1999. The link between phylogeny and virulence in Escherichia coli extra-intestinal infection. Infect. Immun. 67: 546–553.

    PubMed  CAS  Google Scholar 

  • Portaels F. 1987. Le sida et les mycobactérioses atypiques. Ann. Soc. Belge Méd. Trop. 67: 93–113.

    CAS  Google Scholar 

  • Poulin R. 1998. Evolutionary Ecology of Parasites. From Individuals to Communities. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Poulin R. and Combes C. 1999. The concept of virulence: interpretations and implications. Parasitol. Today 15: 474–475.

    Article  PubMed  CAS  Google Scholar 

  • Purvis A. and Rambaut A. 1995. Comparative analysis of independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput. Applied Biosc. 11: 247–251.

    CAS  Google Scholar 

  • Ricklefs R.E. 1996. Applications of phylogenetically independent contrasts: a mixed progress report. Oikos 77: 167–172.

    Google Scholar 

  • Rogall T., Wolters J., Thomas F. and Böttger E.C. 1990. Towards a phylogeny and definition of species at the molecular level within the genus Mycobacterium. Int. J. Syst. Bacteriol. 40: 323–330.

    Article  PubMed  CAS  Google Scholar 

  • Runyon E.H. 1959. Anonymous mycobacteria in pulmonary disease. Med. Clin. North Am. 43: 273–290.

    PubMed  CAS  Google Scholar 

  • Spratt B.G. and Maiden M.C. 1999. Bacterial population genetics, evolution and epidemiology. Phil. Trans. Roy. Soc. Lond. B. Biol. Sc. 354: 701–710.

    Article  CAS  Google Scholar 

  • Springer B., Wu W.K., Bodmer T., Haase G., Pfyffer G.E., Kropenstedt R.M. et al. 1996. Isolation and characterization of a unique group of slowly growing mycobacteria: description of Mycobacterium lenti.avum sp. nov. J. Clin. Microbiol. 34: 1100–1107.

    PubMed  CAS  Google Scholar 

  • Stahl D.A. and Urbance J.W. 1990. The division between fast and slow growing species corresponds to natural relationships among the Mycobacteria. J. Bacteriol. 172: 116–124.

    PubMed  CAS  Google Scholar 

  • Stearns S.C. 1999. Evolution in Health and Disease. Oxford University Press, UK.

    Google Scholar 

  • Swofford D.L. 1993. PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1, Computer Program distributed by the Illinois Natural History Survey. Champaign, Illinois.

  • Thorel M.F., Huchzermeyer H., Weiss R. and Fontaine J.J. 1997. Mycobacterium avium infections in animals. Lit. Rev.,Vet. Res. 28: 439–447.

    CAS  Google Scholar 

  • Tortoli E., Kroppenstedt R.M., Bartoloni A., Caroli G., Jan I., Pawlowski J. et al. 1999. Mycobacterium tusciae sp. nov. Int. J. Syst. Bacteriol. 49: 1839–1844.

    PubMed  CAS  Google Scholar 

  • Tsukamura M. 1984. The nonpathogenic species of Mycobacteria. Their distribution and ecology in non-living reservoirs. In: Kubica G.P. and Wayne L.G. (eds), The Mycobacteria, a Source-book Part B. Marcel Drekker INC, New York and Basel, pp. 1339–1359.

    Google Scholar 

  • Venables W.N. and Ripley B.D. 1994. Modern Applied Statistics with S-Plus. Springer Verlag, Berlin.

    Google Scholar 

  • Vincent Levy-Frebault V. 1991. Ecologie des mycobactéries et mode de contamination humaine. Med. Mal. Infect 21 Sp.: 16–25.

    Article  Google Scholar 

  • Wayne L.G. and Sramek H.A. 1992. Agents of newly recognized or infrequently encountered mycobacterial diseases. Clin. Microbiol. Rev. 5: 1–25.

    PubMed  CAS  Google Scholar 

  • Wilson K. and Grenfell B.T. 1997. Generalized linear modelling for parasitologists. Parasitol. Today 13: 33–38.

    Article  PubMed  CAS  Google Scholar 

  • Zar J.H. 1996. Biostatistical Analysis. 3rd edn. Prentice Hall INC, Upper Saddle River, NJ.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Leclerc, M., Thomas, F. & Guégan, J. Evidence for phylogenetic inheritance in pathogenicity of Mycobacterium . Antonie Van Leeuwenhoek 83, 265–274 (2003). https://doi.org/10.1023/A:1023327929535

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023327929535

Navigation