Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia

Abstract

Many insects that rely on a single food source throughout their developmental cycle harbor beneficial microbes that provide nutrients absent from their restricted diet. Tsetse flies, the vectors of African trypanosomes, feed exclusively on blood and rely on one such intracellular microbe for nutritional provisioning and fecundity. As a result of co-evolution with hosts over millions of years, these mutualists have lost the ability to survive outside the sheltered environment of their host insect cells. We present the complete annotated genome of Wigglesworthia glossinidia brevipalpis, which is composed of one chromosome of 697,724 base pairs (bp) and one small plasmid, called pWig1, of 5,200 bp. Genes involved in the biosynthesis of vitamin metabolites, apparently essential for host nutrition and fecundity, have been retained. Unexpectedly, this obligate's genome bears hallmarks of both parasitic and free-living microbes, and the gene encoding the important regulatory protein DnaA is absent.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Linear representation of the W. glossinidia chromosome illustrating the location of each predicted coding sequences and RNA gene.
Figure 2: Cofactor biosynthetic pathways in W. glossinidia deduced from the gene set.
Figure 3: Genes involved in the synthesis of flagellar assembly of E. coli K12 MG1655.
Figure 4: Comparative analysis of the number of genes present in each functional category described in the genomes of W. glossinidia, Buchnera and R. prowazekii.

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

References

  1. Moran, N.A. & Baumann, P. Endosymbionts in animals. Curr. Opin. Microbiol. 3, 270–275 (2000).

    Article  CAS  Google Scholar 

  2. Aksoy, S. Tsetse: a haven for microorganisms. Parasitol. Today 16, 114–119 (2000).

    Article  CAS  Google Scholar 

  3. Nogge, G. Sterility in tsetse flies (Glossina morsitans Westwood) caused by loss of symbionts. Experientia 32, 995–996 (1976).

    Article  CAS  Google Scholar 

  4. Hill, P.D.S. & Campbell, J.A. The production of symbiont-free Glossina morsitans and an associated loss of female fertility. Trans. R. Soc. Trop. Med. Hyg. 67, 727–728 (1973).

    Article  CAS  Google Scholar 

  5. Nogge, G. Significance of symbionts for the maintenance of an optional nutritional state for successful reproduction in hematophagous arthropods. Parasitology 82, 101–104 (1981).

    Google Scholar 

  6. Aksoy, S. Molecular analysis of the endosymbionts of tsetse flies: 16S rDNA locus and over-expression of a chaperonin. Insect Mol. Biol. 4, 23–29 (1995).

    Article  CAS  Google Scholar 

  7. Chen, X., Song, L. & Aksoy, S. Concordant evolution of a symbiont with its host insect species: Molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J. Mol. Evol. 48, 49–58 (1999).

    Article  CAS  Google Scholar 

  8. Akman, L. & Aksoy, S. A novel application of gene arrays: Escherichia coli array provides insight into the biology of the obligate endosymbiont of tsetse flies. Proc. Natl Acad. Sci. USA 98, 7546–7551 (2001).

    Article  CAS  Google Scholar 

  9. Charles, H. & Ishikawa, H. Physical and genetic map of the genome of Buchnera, the primary endosymbiont of the pea aphid Acrythosiphon pisum. J. Mol. Evol. 48, 142–150 (1999).

    Article  CAS  Google Scholar 

  10. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–86 (2000).

    Article  CAS  Google Scholar 

  11. Fraser, C. et al. The minimal gene complement of Mycoplasma genitalium. Science 270, 397–403 (1995).

    Article  CAS  Google Scholar 

  12. Moran, N.A. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).

    Article  CAS  Google Scholar 

  13. Asai, T. & Kogoma, T. The RecF pathway of homologous recombination can mediate the initiation of DNA damage-inducible replication of the Escherichia coli chromosome. J. Bacteriol. 176, 7113–7114 (1994).

    Article  CAS  Google Scholar 

  14. Douglas, A. Nutritional interactions between Myzus persicae and its symbionts. in Aphid-plant Genotype Interactions (eds Campbell, R. & Eikenbary, R.) 319–327 (Elsevier Biomedical, Amsterdam, the Netherlands, 1990).

    Google Scholar 

  15. Douglas, A.E. & Prosser, W.A. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J. Insect Physiol. 38, 565–568 (1992).

    Article  CAS  Google Scholar 

  16. Ma, W.-C. & Denlinger, D.L. Secretory discharge and microflora of milk gland in tsetse flies. Nature 247, 301–303 (1974).

    Article  Google Scholar 

  17. Cheng, Q. & Aksoy, S. Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol. Biol. 8, 125–132 (1999).

    Article  CAS  Google Scholar 

  18. Kubori, T. et al. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602–605 (1998).

    Article  CAS  Google Scholar 

  19. Young, G.M., Schmiel, D.H. & Miller, V.L. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl Acad. Sci. USA 96, 6456–6461 (1999).

    Article  CAS  Google Scholar 

  20. Andersson, S.G. et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–140 (1998).

    Article  CAS  Google Scholar 

  21. Moloo, S.K. An artificial feeding technique for Glossina. Parasitology 63, 507–512 (1971).

    Article  CAS  Google Scholar 

  22. Sambrook, J. & Russell, D.W. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Press, Cold Spring Harbor, New York, 2001).

    Google Scholar 

  23. O'Neill, S.L., Gooding, R.H. & Aksoy, S. Phylogenetically distant symbiotic microorganisms reside in Glossina midgut and ovary tissues. Med. Vet. Entomol. 7, 377–383 (1993).

    Article  CAS  Google Scholar 

  24. Fleischmann, R.D. et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269, 496–512 (1995).

    Article  CAS  Google Scholar 

  25. Delcher, A.L., Harmon, D., Kasif, S., White, O. & Salzberg, S.L. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27, 4636–4641 (1999).

    Article  CAS  Google Scholar 

  26. Watanabe, H., Mori, H., Itoh, T. & Gojobori, T. Genome plasticity as a paradigm of eubacteria evolution. J. Mol. Evol. 44, S57–S64 (1997).

    Article  CAS  Google Scholar 

  27. Tomb, J.F. et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547 (1997).

    Article  CAS  Google Scholar 

  28. Ogata, H. et al. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 27, 29–34 (1999).

    Article  CAS  Google Scholar 

  29. Kawagishi, I., Muller, V., Williams, A.W., Irikura, V.M. & Macnab, R.M. Subdivision of flagellar region III of the Escherichia coli and Salmonella typhimurium chromosomes and identification of two additional flagellar genes. J. Gen. Microbiol. 138, 1051–1065 (1992).

    Article  CAS  Google Scholar 

  30. Ochman, H. & Groisman, E.A. The origin and evolution of species differences in Escherichia coli and Salmonella typhimurium. EXS 69, 479–493 (1994).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank K. Furuya and C. Yoshino for their technical assistance; I. Kasumba for maintenance of the tsetse colonies; and the members of the Seibersdorf Agricultural Research laboratory, Austria, for their assistance with tsetse pupae. We also thank R.V.M. Rio, D. Nayduch and P. Strickler for their comments and editorial suggestions. This work was supported in part by the Research for the Future Program from the Japanese Society for the Promotion of Science to M.H., the US National Institutes of Health/Nation Institute of Allergy and Infectious Diseases to S.A. and Grant-in-Aid for Scientific Research on Priority Area (C) “Genome Science” from the Ministry of Education, Culture, Sports, Science and Technology of Japan to H.W.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Masahira Hattori or Serap Aksoy.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Akman, L., Yamashita, A., Watanabe, H. et al. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet 32, 402–407 (2002). https://doi.org/10.1038/ng986

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/ng986

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing