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The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism

Abstract

Here we present a draft genome sequence of the nematode Pristionchus pacificus, a species that is associated with beetles and is used as a model system in evolutionary biology. With 169 Mb and 23,500 predicted protein-coding genes, the P. pacificus genome is larger than those of Caenorhabditis elegans and the human parasite Brugia malayi. Compared to C. elegans, the P. pacificus genome has more genes encoding cytochrome P450 enzymes, glucosyltransferases, sulfotransferases and ABC transporters, many of which were experimentally validated. The P. pacificus genome contains genes encoding cellulase and diapausin, and cellulase activity is found in P. pacificus secretions, indicating that cellulases can be found in nematodes beyond plant parasites. The relatively higher number of detoxification and degradation enzymes in P. pacificus is consistent with its necromenic lifestyle and might represent a preadaptation for parasitism. Thus, comparative genomics analysis of three ecologically distinct nematodes offers a unique opportunity to investigate the association between genome structure and lifestyle.

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Figure 1: Phylogeny and comparison of genomic features in nematodes.
Figure 2: Orthology assignment in nematodes and comparison to non-nematode species.
Figure 3: Examples of P. pacificus–specific expansions.
Figure 4: Schematic representation of the metabolism of xenobiotics.
Figure 5: Cellulase activity in P. pacificus.

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References

  1. The C. elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: A platform for investigating biology. Science 282, 2012–2018 (1998).

  2. Kiontke, K. & Sudhaus, W. Ecology of Caenorhabditis species. in WormBook ed. (The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.37.1, 2006).

  3. Ghedin, E. et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 1756–1760 (2007).

    Article  CAS  Google Scholar 

  4. Sommer, R.J., Carta, L.K., Kim, S.-Y. & Sternberg, P.W. Morphological, genetic and molecular description of Pristionchus pacificus sp. n. Fundam. Appl. Nematol. 19, 511–521 (1996).

    Google Scholar 

  5. Hong, R.L. & Sommer, R.J. Pristionchus pacificus: a well rounded nematode. Bioessays 28, 651–659 (2006).

    Article  CAS  Google Scholar 

  6. Zheng, M., Messerschmidt, D., Jungblut, B. & Sommer, R.J. Conservation and diversification of Wnt signaling function during the evolution of nematode vulva development. Nat. Genet. 37, 300–304 (2005).

    Article  CAS  Google Scholar 

  7. Schlager, B., Röseler, W., Zheng, M., Gutierrez, A. & Sommer, R.J. HAIRY-like transcription factors and the evolution of the nematode vulva equivalence group. Curr. Biol. 16, 1386–1394 (2006).

    Article  CAS  Google Scholar 

  8. Yi, B. & Sommer, R.J. The pax-3 gene is involved in vulva formation in Pristionchus pacificus and is a target of the Hox gene lin-39. Development 134, 3111–3119 (2007).

    Article  CAS  Google Scholar 

  9. Tian, H., Schlager, B., Xiao, H. & Sommer, R.J. Wnt signaling by differentially expressed Wnt ligands induces vulva development in Pristionchus pacificus. Curr. Biol. 18, 142–146 (2008).

    Article  CAS  Google Scholar 

  10. Herrmann, M. et al. The nematode Pristionchus pacificus is associated with the oriental beetle Exomala orientalis in Japan. Zoolog. Sci. 24, 883–889 (2007).

    Article  CAS  Google Scholar 

  11. Srinivasan, J. et al. A bacterial artificial chromosome-based genetic linkage map of the nematode Pristionchus pacificus. Genetics 162, 129–134 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Mayer, W.E., Herrmann, M. & Sommer, R.J. Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism. BMC Evol. Biol. 7, 104 (2007).

    Article  Google Scholar 

  13. Stanke, M. & Waack, S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19 Suppl 2, ii215–ii225 (2003).

    Article  Google Scholar 

  14. Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).

    Article  Google Scholar 

  15. Majoros, W.H., Pertea, M. & Salzberg, S.L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879 (2004).

    Article  CAS  Google Scholar 

  16. Alexeyenko, A., Tamas, I., Liu, G. & Sonnhammer, E.L.L. Automatic clustering of orthologs and inparalogs shared by multiple proteomes. Bioinformatics 22, e9–e15 (2006).

    Article  CAS  Google Scholar 

  17. Finn, R.D. et al. The Pfam protein family database. Nucleic Acids Res. 36, D281–D288 (2008).

    Article  CAS  Google Scholar 

  18. Kanehisa, M. et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36, D480–D484 (2008).

    Article  CAS  Google Scholar 

  19. Stein, L.D. et al. The genome sequence of Caenorhabditis briggsae: A platform for comparative genomics. PLoS Biol. 1, 166–192 (2003).

    Article  CAS  Google Scholar 

  20. Oesch, F. & Arand, M. Xenobiotic metabolism. in Toxicology Marquardt, H. et al. (eds.) Academic Press, San Diego, pp. 83–107 (1999).

    Chapter  Google Scholar 

  21. Smant, G. et al. Endogenous cellulases in animals: isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc. Natl. Acad. Sci. USA 95, 4906–4911 (1998).

    Article  CAS  Google Scholar 

  22. Kikuchi, T., Jones, J.T., Aikawa, T., Kosaka, H. & Ogura, N. A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Lett. 572, 201–205 (2004).

    Article  CAS  Google Scholar 

  23. Keen, N.T. & Roberts, P.A. Plant parasitic nematodes: digesting a page from the microbe book. Proc. Natl. Acad. Sci. USA 95, 4789–4790 (1998).

    Article  CAS  Google Scholar 

  24. Tanaka, H. et al. Insect diapause-specific peptide from the leaf beetle has consensus with a putative iridovirus peptide. Peptides 24, 1327–1333 (2003).

    Article  CAS  Google Scholar 

  25. Dunning Hotopp, J.C. et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–1756 (2007).

    Article  CAS  Google Scholar 

  26. Blaxter, M. Symbiont genes in host genomes: fragments with a future. Cell Host Microbe 2, 211–213 (2007).

    Article  CAS  Google Scholar 

  27. Blaxter, M. et al. A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75 (1998).

    Article  CAS  Google Scholar 

  28. Weischer, B. & Brown, D.J.F. An Introduction to Nematodes (Pensoft, Moscow, 2000).

    Google Scholar 

  29. Poulin, R. Evolutionary Ecology of Parasites (Princeton University Press, Princeton, New Jersey, 2007).

    Google Scholar 

  30. Huang, X. et al. Application of a superword array in genome assembly. Nucleic Acids Res. 34, 201–205 (2006).

    Article  CAS  Google Scholar 

  31. Bao, Z. & Eddy, S.R. Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res. 12, 1269–1276 (2002).

    Article  CAS  Google Scholar 

  32. Huang, X. & Madan, A. CAP3: A DNA sequence assembly program. Genome Res. 9, 868–877 (1999).

    Article  CAS  Google Scholar 

  33. Slater, G.S.C. & Birney, E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005).

    Article  Google Scholar 

  34. Allen, J.E., Majoros, W.H., Pertea, M. & Salzberg, S.L. JIGSAW, GeneZilla, and GlimmerHMM: puzzling out the features of human genes in the ENCODE regions. Genome Biol 7 Suppl 1, S9.1–S9.13 (2006).

    Article  Google Scholar 

  35. Remm, M., Storm, C.E. & Sonnhammer, E.L. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J. Mol. Biol. 314, 1041–1052 (2001).

    Article  CAS  Google Scholar 

  36. Enright, A.J., Dongen, S.V. & Ouzounis, C.A. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30, 1575–1584 (2002).

    Article  CAS  Google Scholar 

  37. Sanderson, M.J. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14, 1218–1231 (1997).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank P.W. Sternberg, J. Srinivasan and members of the Sommer lab for discussion and helpful comments on the manuscript. This work was funded by National Human Genome Research Institute grant U54HG003079 and the Max-Planck Society.

Author information

Authors and Affiliations

Authors

Contributions

C.D. carried out most of the bioinformatics analysis; the Genome Sequencing Center team at Washington University (S.W.C., A.C., K.D., L.F., R.F., J.G., P.M., M.M., S.-P.Y., R.K.W.) conducted the genome sequencing project; L.N.S. and H.T. did the experimental gene confirmation; I.D., W.R. and H.W. experimentally linked the genetic linkage map to the P. pacificus genome; and C.D., S.W.C., R.K.W. and R.J.S. designed these studies and contributed to the writing of this paper.

Corresponding authors

Correspondence to Richard K Wilson or Ralf J Sommer.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6 (PDF 708 kb)

Supplementary Table 1

Repeat family annotation. (XLS 2669 kb)

Supplementary Table 2

Gene modeller performance. (XLS 155 kb)

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Dieterich, C., Clifton, S., Schuster, L. et al. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 40, 1193–1198 (2008). https://doi.org/10.1038/ng.227

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