Skip to main content
SpringerLink
Log in

Pneumocystis carinii Subtelomeres

  • Chapter
  • First Online:
Subtelomeres

Abstract

Pneumocystis carinii is a yeast-like fungus that dwells exclusively in rats, where it is subjected to the host immune response. Immune pressure is countered by three subtelomeric gene families that generate antigenic diversity in populations of P. carinii. Members of the three gene families are grouped together in tandem arrays that appear to have been generated by recombination and modified by further recombination events after array formation. One of these gene families, MSG, encodes various forms of a major surface glycoprotein. In a given P. carinii organism, all but one of the members of the MSG gene family appear to be transcriptionally silent. The expressed MSG gene is adjacent to a unique locus (the expression site). Different MSG genes can occupy the expression site, suggesting that recombination can take a gene from a pool of silent donors and install it at the expression site, thereby extinguishing transcription of the previous expression site resident, activating transcription of the newly installed MSG gene, and changing the surface of the microbe. Switching at the expression site is probably facilitated by the subtelomeric locations of expressed and silent MSG genes. A second subtelomeric gene family, MSR, is not strictly regulated at the transcriptional level, but may contribute to phenotypic diversity via high-frequency frameshifting caused by coding poly(G) tracts in some MSR genes.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aliouat-Denis, C. M., Chabe, M., Demanche, C., Aliouat, E. M., Viscogliosi, E., Guillot, J., et al. (2008). Pneumocystis species, co-evolution and pathogenic power. Infection, Genetics and Evolution, 8, 708–726.

    Article  PubMed  Google Scholar 

  • Ambrose, H. E., Keely, S. P., Aliouat, E. M., Dei-Cas, E., Wakefield, A. E., Miller, R. F., et al. (2004). Expression and complexity of the PRT1 multigene family of Pneumocystis carinii. Microbiology, 150, 293–300.

    Article  CAS  PubMed  Google Scholar 

  • Barry, J. D., Ginger, M. L., Burton, P., & McCulloch, R. (2003). Why are parasite contingency genes often associated with telomeres? International Journal for Parasitology, 33, 29–45.

    Article  CAS  PubMed  Google Scholar 

  • Brubaker, R., Redhead, S. A., Stringer, J. R., Keely, S. P., & Cushion, M. T. (2009). Misinformation about Pneumocystis. Clinical and Experimental Dermatology, 34, e426–e427.

    Article  CAS  PubMed  Google Scholar 

  • Cornillot, E., Keller, B., Cushion, M. T., Metenier, G., & Vivares, C. P. (2002). Fine analysis of the Pneumocystis carinii f. sp. carinii genome by two- dimensional pulsed-field gel electrophoresis. Gene, 293, 87–95.

    Article  CAS  PubMed  Google Scholar 

  • Cushion, M. T. (1998). Genetic heterogeneity of rat-derived Pneumocystis. FEMS Immunology and Medical Microbiology, 22, 51–58.

    Article  CAS  PubMed  Google Scholar 

  • Cushion, M. T., & Stringer, J. R. (2005). Has the name really been changed? it has for most researchers. Clinical Infectious Diseases, 41, 1756–1758.

    Article  PubMed  Google Scholar 

  • Cushion, M. T., & Stringer, J. R. (2010). Stealth and opportunism: Alternative lifestyles of species in the fungal genus Pneumocystis. Annual Review of Microbiology, 64, 431–452.

    Article  CAS  PubMed  Google Scholar 

  • Cushion, M. T., Keely, S. P., & Stringer, J. R. (2004). Molecular and phenotypic description of Pneumocystis wakefieldiae sp. nov., a new species in rats. Mycologia, 96, 429–438.

    Article  CAS  PubMed  Google Scholar 

  • Cushion, M. T., Keely, S. P., & Stringer, J. R. (2005). Validation of the name Pneumocystis wakefieldiae. Mycologia, 97, 268.

    Article  Google Scholar 

  • Cushion, M. T., Smulian, A. G., Slaven, B. E., Sesterhenn, T., Arnold, J., Staben, C., et al. (2007). Transcriptome of Pneumocystis carinii during fulminate infection: Carbohydrate metabolism and the concept of a compatible parasite. PLoS ONE, 2, e423.

    Article  PubMed Central  PubMed  Google Scholar 

  • Dei-Cas, E., Chabe, M., Moukhlis, R., Durand-Joly, I., Aliouat, E. M., Stringer, J. R., et al. (2006). Pneumocystis oryctolagi sp. nov., an uncultured fungus causing pneumonia in rabbits at weaning: Review of current knowledge, and description of a new taxon on genotypic, phylogenetic and phenotypic bases. FEMS Microbiology Reviews, 30, 853–871.

    Article  CAS  PubMed  Google Scholar 

  • Deitsch, K. W., Lukehart, S. A., & Stringer, J. R. (2009). Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nature Reviews Microbiology, 7, 493–503.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • DePrimo, S. E., Cao, J., Hersh, M. N., & Stringer, J. R. (1998). Use of human placental alkaline phosphatase transgenes to detect somatic mutation in mice in situ. Methods, 16, 49–61.

    Article  CAS  PubMed  Google Scholar 

  • Durand-Joly, I., Aliouat, E. M., Recourt, C., Guyot, K., Francois, N., Wauquier, M., et al. (2002). Pneumocystis carinii f. sp. hominis is not infectious for SCID mice. Journal of Clinical Microbiology, 40, 1862–1865.

    Article  PubMed Central  PubMed  Google Scholar 

  • Edman, J. C., Hatton, T. W., Nam, M., Turner, R., Mei, Q., Angus, C. W., et al. (1996). A single expression site with a conserved leader sequence regulates variation of expression of the Pneumocystis carinii family of major surface glycoprotein genes. DNA and Cell Biology, 15, 989–999.

    Article  CAS  PubMed  Google Scholar 

  • Eriksson, O. E. (1994). Pneumocystis carinii, a parasite in lungs of mammals, referred to a new family and order (Pneumocystidaceae, Pneumocystidales, Ascomycota). Systema Ascomycetum, 13, 165–180.

    Google Scholar 

  • Fischer, J. M., Keely, S. P., & Stringer, J. R. (2006). Evolutionary rate of Ribosomal DNA in Pneumocystis species is normal despite the extraordinarily low copy-number of rDNA genes. Journal of Eukaryotic Microbiology, 53(Suppl 1), S156–S158.

    Article  CAS  PubMed  Google Scholar 

  • Garbe, T. R., & Stringer, J. R. (1994). Molecular characterization of clustered variants of genes encoding major surface antigens of human Pneumocystis carinii. Infection and Immunity, 62, 3092–3101.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gigliotti, F., Harmsen, A. G., Haidaris, C. G., & Haidaris, P. J. (1993). Pneumocystis carinii is not universally transmissible between mammalian species. Infection and Immunity, 61, 2886–2890.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haidaris, C. G., Medzihradsky, O. F., Gigliotti, F., & Simpson-Haidaris, P. J. (1998). Molecular characterization of mouse Pneumocystis carinii surface glycoprotein A. DNA Research, 5, 77–85.

    Article  CAS  PubMed  Google Scholar 

  • Hersh, M. N., Stambrook, P. J., & Stringer, J. R. (2002). Visualization of mosaicism in tissues of normal and mismatch-repair-deficient mice carrying a microsatellite-containing transgene. Mutation Research, 505, 51–62.

    Article  CAS  PubMed  Google Scholar 

  • Huang, S. N., Angus, C. W., Turner, R. E., Sorial, V., & Kovacs, J. A. (1999). Identification and characterization of novel variant major surface glycoprotein gene families in rat Pneumocystis carinii. Journal of Infectious Diseases, 179, 192–200.

    Article  CAS  PubMed  Google Scholar 

  • Huang, L., Cattamanchi, A., Davis, J. L., den, B. S., Kovacs, J., Meshnick, S., et al. (2011). HIV-associated Pneumocystis pneumonia. Proceedings of the American Thoracic Society, 8, 294–300.

    Article  PubMed Central  PubMed  Google Scholar 

  • Keely, S. P., & Stringer, J. R. (2003). Sequence diversity of transcripts from Pneumocystis carinii gene families MSR and PRT1. Journal of Eukaryotic Microbiology, 50(Suppl), 627–628.

    Article  CAS  PubMed  Google Scholar 

  • Keely, S. P., & Stringer, J. R. (2005). Nomenclature and genetic variation of Pneumocystis. Pneumocystis Pneumonia, 3, 39–59.

    Google Scholar 

  • Keely, S. P., & Stringer, J. R. (2009). Complexity of the MSG gene family of Pneumocystis carinii. BMC Genomics, 10, 367.

    Article  PubMed Central  PubMed  Google Scholar 

  • Keely, S. P., Baughman, R. P., Smulian, A. G., Dohn, M. N., & Stringer, J. R. (1996). Source of Pneumocystis carinii in recurrent episodes of pneumonia in AIDS patients. AIDS, 10, 881–888.

    Article  CAS  PubMed  Google Scholar 

  • Keely, S. P., Cushion, M. T., & Stringer, J. R. (1999). Determination of the maximum frequency of genetic rearrangements associated with Pneumocystis carinii surface antigen variation (In Process Citation). Journal of Eukaryotic Microbiology, 46, 128S.

    CAS  PubMed  Google Scholar 

  • Keely, S. P., Fischer, J. M., & Stringer, J. R. (2003). Evolution and speciation of Pneumocystis. Journal of Eukaryotic Microbiology, 50(Suppl), 624–626.

    Article  CAS  PubMed  Google Scholar 

  • Keely, S. P., Fischer, J. M., Cushion, M. T., & Stringer, J. R. (2004). Phylogenetic identification of Pneumocystis murina sp. nov., a new species in laboratory mice. Microbiology, 150, 1153–1165.

    Article  CAS  PubMed  Google Scholar 

  • Keely, S. P., Renauld, H., Wakefield, A. E., Cushion, M. T., Smulian, A. G., Fosker, N., et al. (2005). Gene arrays at Pneumocystis carinii telomeres. Genetics, 170, 1589–1600.

    Article  CAS  PubMed  Google Scholar 

  • Keely, S. P., Linke, M. J., Cushion, M. T., & Stringer, J. R. (2007). Pneumocystis murina MSG gene family and the structure of the locus associated with its transcription. Fungal Genetics and Biology, 44, 905–919.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kutty, G., & Kovacs, J. A. (2003). A single-copy gene encodes Kex1, a serine endoprotease of Pneumocystis jiroveci. Infection and Immunity, 71, 571–574.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kutty, G., Huang, S. N., & Kovacs, J. A. (2003). Characterization of thioredoxin reductase genes (trr1) from Pneumocystis carinii and Pneumocystis jiroveci. Gene, 310, 175–183.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Leigh, J. W., Brinkmann, H., Cushion, M. T., Rodriguez-Ezpeleta, N., Philippe, H., et al. (2009). Phylogenomic analyses support the monophyly of Taphrinomycotina, including Schizosaccharomyces fission yeasts. Molecular Biology and Evolution, 26, 27–34.

    Article  PubMed  Google Scholar 

  • Lugli, E. B., Allen, A. G., & Wakefield, A. E. (1997). A Pneumocystis carinii multi-gene family with homology to subtilisin-like serine proteases. Microbiology, 143, 2223–2236.

    Article  CAS  PubMed  Google Scholar 

  • Miller, R. F. (1999). Pneumocystis carinii infection in non-AIDS patients. Current opinion in infectious diseases, 12, 371–377.

    Article  CAS  PubMed  Google Scholar 

  • Rebholz, S. L., & Cushion, M. T. (2001). Three new karyotype forms of Pneumocystis carinii f. sp. carinii identified by contoured clamped homogeneous electrical field (CHEF) electrophoresis. Journal of Eukaryotic Microbiology, 48(Suppl), 109S–110S.

    Google Scholar 

  • Redhead, S. A., Cushion, M. T., Frenkel, J. K., & Stringer, J. R. (2006). Pneumocystis and Trypanosoma cruzi: Nomenclature and Typifications. Journal of Eukaryotic Microbiology, 53, 2–11.

    Article  PubMed  Google Scholar 

  • Russian, D. A., Andrawis-Sorial, V., Goheen, M. P., Edman, J. C., Vogel, P., Turner, R. E., et al. (1999). Characterization of a multicopy family of genes encoding a surface- expressed serine endoprotease in rat Pneumocystis carinii. Proceedings of the Association of American Physicians, 111, 347–356.

    Article  CAS  PubMed  Google Scholar 

  • Schaffzin, J. K., & Stringer, J. R. (2000). The major surface glycoprotein expression sites of two special forms of rat Pneumocystis carinii differ in structure. Journal of Infectious Diseases, 181, 1729–1739.

    Article  CAS  PubMed  Google Scholar 

  • Schaffzin, J. K., & Stringer, J. R. (2004). Expression of the Pneumocystis carinii major surface glycoprotein epitope is correlated with linkage of the cognate gene to the upstream conserved sequence locus. Microbiology, 150, 677–686.

    Article  CAS  PubMed  Google Scholar 

  • Schaffzin, J. K., Garbe, T. R., & Stringer, J. R. (1999a). Major surface glycoprotein genes from pneumocystis carinii f. sp. ratti. Fungal Genetics and Biology, 28, 214–226.

    Article  CAS  PubMed  Google Scholar 

  • Schaffzin, J. K., Sunkin, S. M., & Stringer, J. R. (1999b). A new family of Pneumocystis carinii genes related to those encoding the major surface glycoprotein. Current Genetics, 35, 134–143.

    Article  CAS  PubMed  Google Scholar 

  • Sethi, K. K. (1992). Multiplication of human-derived Pneumocystis carinii in severe combined immunodeficient (SCID) mice. Experientia, 48, 63–66.

    Article  CAS  PubMed  Google Scholar 

  • Smulian, A. G., Linke, M. J., Cushion, M. T., Baughman, R. P., Frame, P. T., Dohn, M. N., et al. (1994). Analysis of Pneumocystis carinii organism burden, viability and antigens in bronchoalveolar lavage fluid in AIDS patients with pneumocystosis: Correlation with disease severity. AIDS, 8, 1555–1562.

    Article  CAS  PubMed  Google Scholar 

  • Smulian, A. G., Sesterhenn, T., Tanaka, R., & Cushion, M. T. (2001). The ste3 pheromone receptor gene of Pneumocystis carinii Is surrounded by a cluster of signal transduction genes. Genetics, 157, 991–1002.

    CAS  PubMed  Google Scholar 

  • Stringer, J. R. (1994). Molecular Genetics of Pneumocystis carinii. In P. D. Walzer (Ed.), Pneumocystis carinii pneumonia (2nd ed., pp.73–90). Inc., New York: Marcel Dekker.

    Google Scholar 

  • Stringer, J. R. (2002). Pneumocystis. International Journal of Medical Microbiology, 292, 391–404.

    Article  CAS  PubMed  Google Scholar 

  • Stringer, J. R. (2003). The MSG gene family and antigenic variation in the fungus P. carinii. In A. Craig, A. Scherf (Eds.), Antigenic Variation (pp. 201–223). Amsterdam: Academic Press.

    Google Scholar 

  • Stringer, J. R. (2007). Antigenic variation in Pneumocystis. Journal of Eukaryotic Microbiology, 54, 8–13.

    Article  CAS  PubMed  Google Scholar 

  • Stringer, J. R., & Cushion, M. T. (1998). The genome of Pneumocystis carinii. FEMS Immunology and Medical Microbiology, 22, 15–26.

    Article  CAS  PubMed  Google Scholar 

  • Stringer, J. R., & Keely, S. P. (2001). Genetics of surface antigen expression in Pneumocystis carinii. Infection and Immunity, 69, 627–639.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stringer, S. L., Hong, S. T., Giuntoli, D., & Stringer, J. R. (1991). Repeated DNA in Pneumocystis carinii. Journal of Clinical Microbiology, 29, 1194–1201.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stringer, S. L., Garbe, T., Sunkin, S. M., & Stringer, J. R. (1993). Genes encoding antigenic surface glycoproteins in Pneumocystis from humans. Journal of Eukaryotic Microbiology, 40, 821–826.

    Article  CAS  PubMed  Google Scholar 

  • Stringer, J. R., Beard, C. B., Miller, R. F., & Wakefield, A. E. (2002). A new name (Pneumocystis jirovecii) for Pneumocystis from humans. Emerging Infectious Diseases, 8, 891–896.

    Article  PubMed  Google Scholar 

  • Stringer, J. R., Cushion, M. T., & Redhead, S. A. (2006). Reply to weinberg, to hughes, and to limper. Clinical Infectious Diseases, 42, 1212–1214.

    Article  Google Scholar 

  • Stringer, J. R., Beard, C. B., & Miller, R. F. (2009). Spelling Pneumocystis jirovecii. Emerging Infectious Diseases, 15, 506.

    Article  PubMed  Google Scholar 

  • Sunkin, S. M., & Stringer, J. R. (1996). Translocation of surface antigen genes to a unique telomeric expression site in Pneumocystis carinii. Molecular Microbiology, 19, 283–295.

    Article  CAS  PubMed  Google Scholar 

  • Sunkin, S. M., & Stringer, J. R. (1997). Residence at the expression site is necessary and sufficient for the transcription of surface antigen genes of Pneumocystis carinii. Molecular Microbiology, 25, 147–160.

    Article  CAS  PubMed  Google Scholar 

  • Sunkin, S. M., Linke, M. J., McCormack, F. X., Walzer, P. D., & Stringer, J. R. (1998). Identification of a putative precursor to the major surface glycoprotein of Pneumocystis carinii. Infection and Immunity, 66, 741–746.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thomas, C. F, Jr, Leof, E. B., & Limper, A. H. (1999). Analysis of Pneumocystis carinii introns. Infection and Immunity, 67, 6157–6160.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Underwood, A. P., Louis, E. J., Borts, R. H., Stringer, J. R., & Wakefield, A. E. (1996). Pneumocystis carinii telomere repeats are composed of TTAGGG and the subtelomeric sequence contains a gene encoding the major surface glycoprotein. Molecular Microbiology, 19, 273–281.

    Article  CAS  PubMed  Google Scholar 

  • Wada, M., & Nakamura, Y. (1994). MSG gene cluster encoding major cell surface glycoproteins of rat Pneumocystis carinii. DNA Research, 1, 163–168.

    Article  CAS  PubMed  Google Scholar 

  • Wada, M., & Nakamura, Y. (1996). Unique telomeric expression site of major-surface-glycoprotein genes of Pneumocystis carinii. DNA Research, 3, 55–64.

    Article  CAS  PubMed  Google Scholar 

  • Wada, M., Sunkin, S. M., Stringer, J. R., & Nakamura, Y. (1995). Antigenic variation by positional control of major surface glycoprotein gene expression in Pneumocystis carinii. Journal of Infectious Diseases, 171, 1563–1568.

    Article  CAS  PubMed  Google Scholar 

  • Wright, T. W., Simpson Haidaris, P. J., Gigliotti, F., Harmsen, A. G., & Haidaris, C. G. (1994). Conserved sequence homology of cysteine-rich regions in genes encoding glycoprotein A in Pneumocystis carinii derived from different host species. Infection and Immunity, 62, 1513–1519.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wright, T. W., Bissoondial, T. Y., Haidaris, C. G., Gigliotti, F., & Haidaris, P. J. (1995a). Isoform diversity and tandem duplication of the glycoprotein A gene in ferret Pneumocystis carinii. DNA Research, 2, 77–88.

    Article  CAS  PubMed  Google Scholar 

  • Wright, T. W., Gigliotti, F., Haidaris, C. G., & Simpson-Haidaris, P. J. (1995b). Cloning and characterization of a conserved region of human and rhesus macaque Pneumocystis carinii gpA. Gene, 167, 185–189.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to thank Saundra Stringer, Ann Wakefield, and Scott Keely for their help and encouragement as the work on Pneumocystis telomeres began, developed, and matured.

Author information

Authors and Affiliations

  1. Department of Molecular Genetics, Biochemistry and Microbiology, University of Cincinnati, Cincinnati, OH, 45220-0524, USA

    James R. Stringer

Authors
  1. James R. Stringer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James R. Stringer .

Editor information

Editors and Affiliations

  1. Department of Genetics, University of Leicester, Leicester, United Kingdom

    Edward J Louis

  2. Department of Genetics, University of Leicester, Leicester, United Kingdom

    Marion M Becker

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Stringer, J.R. (2014). Pneumocystis carinii Subtelomeres. In: Louis, E., Becker, M. (eds) Subtelomeres. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-41566-1_5

Download citation

Publish with us

Policies and ethics

Search

Navigation