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Evolutionary Biology

, Volume 37, Issue 1, pp 29–37 | Cite as

Using Algal Transcriptome Sequences to Identify Transferred Genes in the Sea Slug, Elysia chlorotica

  • Julie A. SchwartzEmail author
  • Nicholas E. Curtis
  • Sidney K. Pierce
Research Article
First Online:

Abstract

The first molecular evidence of horizontal gene transfer between multicellular eukaryotes was our discovery of the presence of three Vaucheria litorea nuclear-encoded genes [fucoxanthin chlorophyll a/c-binding protein (fcp) and light-harvesting complex 1 and 2 (Lhcv1 and 2)] in the genomic DNA of the sea slug, Elysia chlorotica, which are used to support the chloroplast endosymbiosis in the slug. These genes are translated and transcribed in the host cell, and vertically transmitted to subsequent generations of the host species. In order to provide a database of native V. litorea sequences to facilitate the search for additional transferred genes between these two species, we have partially sequenced and annotated the transcriptome of V. litorea, using 454 Life Science’s next generation pyrosequencing technology. Preliminary analysis of the sequence data has led to the discovery of six additional algal nuclear genes in E. chlorotica cDNA and genomic DNA, which encode enzymes in the chlorophyll synthesis pathway as well as additional light-harvesting and metabolic enzymes. Furthermore, we confirm the recent discovery of the Calvin-Benson cycle gene, prk.

Keywords

Horizontal gene transfer Transcriptome analysis Chloroplast endosymbiosis Vaucheria litorea Elysia chlorotica Kleptoplasty 
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Notes

Acknowledgements

We are grateful for a generous financial donation to support this research from a donor who wishes to remain anonymous. We would not have been able to do the work presented here without that person’s help.

References

  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.PubMedGoogle Scholar
  2. Clark, K. B., Jensen, K. R., & Stirts, H. M. (1990). Survey of functional kleptoplasty among west Atlantic Ascoglossa (= Sacoglossa) (Mollusca:Opisthobranchia). The Veliger, 33, 339–345.Google Scholar
  3. Darling, A., Carey, L., & Feng, W. (2003). The design, implementation, and evaluation of mpiBLAST. In 4th international conference on linux clusters: The HPC revolution 2003 in conjunction with clusterworld conference & expo, 2003 June.Google Scholar
  4. Eberhard, S., Finazzi, G., & Wollman, F. A. (2008). The dynamics of photosynthesis. Annual Review of Genetics, 42, 463–515.CrossRefPubMedGoogle Scholar
  5. Evertsen, J., Burghardt, I., Johnsen, G., & Wägele, H. (2007). Retention of functional chloroplasts in some sacoglossans from the Indo-Pacific and Mediterranean. Marine Biology, 151, 2159–2166.CrossRefGoogle Scholar
  6. Gould, S. B., Waller, R. F., & McFadden, G. I. (2008). Plastid Evolution. Annual Review of Plant Biology, 59, 491–517.CrossRefPubMedGoogle Scholar
  7. Green, B. J., Wei-Ye, L., Manhart, J. R., Fox, T. C., Summer, E. J., Kennedy, R. A., et al. (2000). Mollusc-algal chloroplast endosymbiosis. Photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiology, 124, 331–342.CrossRefPubMedGoogle Scholar
  8. Hinde, R., & Smith, D. C. (1974). “Chloroplast symbiosis” and the extent to which it occurs in Sacoglossa (Gastropoda:mollusca). Biological Journal of the Linnean Society, 6, 349–356.CrossRefGoogle Scholar
  9. Kleine, T., Voigt, C., & Leister, D. (2009). Plastid signalling to the nucleus: Messengers still lost in the mists? Trends in Genetics, 25, 185–192.CrossRefPubMedGoogle Scholar
  10. Lin, H., Ma, X., Chandramohan, P., Geist, A., & Samatova, N. (2005). Efficient Data Access for Parallel BLAST. In: Proceedings of 19th international parallel & distributed processing symposium, April 3–8, 2005, Denver, CO.Google Scholar
  11. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., & Bader, J. S. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376–380.PubMedGoogle Scholar
  12. Masuda, T., & Fujita, Y. (2008). Regulation and evolution of chlorophyll metabolism. Photochemical & Photobiological Sciences, 7, 1131–1149.CrossRefGoogle Scholar
  13. Mondy, W. L., & Pierce, S. K. (2003). Apoptotic-like morphology is associated with annual synchronized death in kleptoplastic sea slugs (Elysia chlorotica). Invertebrate Biology, 122, 126–137.CrossRefGoogle Scholar
  14. Pesaresi, P., Schneider, A., Kleine, T., & Leister, D. (2007). Interorganellar communication. Current Opinion in Plant Biology, 10, 600–606.CrossRefPubMedGoogle Scholar
  15. Pierce, S. K., Biron, R. W., & Rumpho, M. E. (1996). Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. Journal of Experimental Biology, 199, 2323–2330.PubMedGoogle Scholar
  16. Pierce, S. K., Curtis, N. E., Hanten, J. J., Boerner, S. L., & Schwartz, J. A. (2007). Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis, 43, 57–64.Google Scholar
  17. Pierce, S. K., Curtis, N. E., & Schwartz, J. A. (2009). Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis, 49, 121–131.CrossRefGoogle Scholar
  18. Pierce, S. K., Maugel, T. K., Rumpho, M. E., Hanten, J. J., & Mondy, W. L. (1999). Annual viral expression in a sea slug population: Life cycle control and symbiotic chloroplast maintenance. Biological Bulletin, 197, 1–6.CrossRefGoogle Scholar
  19. Rumpho, M. E., Pochareddy, S., Worful, J. M., Summer, E. J., Bhattacharya, D., Pelletreau, K. N., et al. (2009). Molecular characterization of the Calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. Molecular Plant, 2, 1384–1396.CrossRefPubMedGoogle Scholar
  20. Rumpho, M. E., Summer, E. J., Green, B. J., Fox, T. C., & Manhart, J. R. (2001). Mollusc/algal chloroplast symbiosis: How can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus? Zoology, 104, 303–312.CrossRefPubMedGoogle Scholar
  21. Rumpho, M. E., Worful, J. M., Lee, J., Kannan, K., Tyler, M. S., Bhattacharya, D., et al. (2008). Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proceedings of the National Academy of Science of the United States of America, 105, 17867–17871.CrossRefGoogle Scholar
  22. Tanaka, R., & Tanaka, A. (2007). Tetrapyrrole biosynthesis in higher plants. Annual Review of Plant Biology, 58, 321–346.CrossRefPubMedGoogle Scholar
  23. Trench, R. K. (1969). Chloroplasts as functional organelles in animal tissues. Nature, 222, 1071–1072.CrossRefGoogle Scholar
  24. Wägele, H., & Johnsen, G. (2001). Observations on the histology and photosynthetic performance of “solar-powered” opisthobranchs (Mollusca, Gastropoda, Opisthobranchia) containing symbiotic chloroplasts or zooxanthellae. Organisms, Diversity & Evolution, 1, 193–210.CrossRefGoogle Scholar
  25. West, H. H., Harrigan, J. F., & Pierce, S. K. (1984). Hybridization of two populations of marine opisthobranch with different developmental patterns. The Veliger, 26, 199–206.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Julie A. Schwartz
    • 1
    Email author
  • Nicholas E. Curtis
    • 1
  • Sidney K. Pierce
    • 1
  1. 1.Department of Integrative BiologyUniversity of South FloridaTampaUSA

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