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

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.

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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.

    CAS  PubMed  Google 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.

  4. Eberhard, S., Finazzi, G., & Wollman, F. A. (2008). The dynamics of photosynthesis. Annual Review of Genetics, 42, 463–515.

    Article  CAS  PubMed  Google 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.

    Article  Google Scholar 

  6. Gould, S. B., Waller, R. F., & McFadden, G. I. (2008). Plastid Evolution. Annual Review of Plant Biology, 59, 491–517.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  Google 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.

    Article  CAS  PubMed  Google 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.

  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.

    CAS  PubMed  Google Scholar 

  12. Masuda, T., & Fujita, Y. (2008). Regulation and evolution of chlorophyll metabolism. Photochemical & Photobiological Sciences, 7, 1131–1149.

    Article  CAS  Google 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.

    Article  Google Scholar 

  14. Pesaresi, P., Schneider, A., Kleine, T., & Leister, D. (2007). Interorganellar communication. Current Opinion in Plant Biology, 10, 600–606.

    Article  CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  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.

    Article  Google 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.

    Article  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  Google Scholar 

  22. Tanaka, R., & Tanaka, A. (2007). Tetrapyrrole biosynthesis in higher plants. Annual Review of Plant Biology, 58, 321–346.

    Article  CAS  PubMed  Google Scholar 

  23. Trench, R. K. (1969). Chloroplasts as functional organelles in animal tissues. Nature, 222, 1071–1072.

    Article  Google 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.

    Article  Google 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 

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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.

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Correspondence to Julie A. Schwartz.

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Schwartz, J.A., Curtis, N.E. & Pierce, S.K. Using Algal Transcriptome Sequences to Identify Transferred Genes in the Sea Slug, Elysia chlorotica . Evol Biol 37, 29–37 (2010). https://doi.org/10.1007/s11692-010-9079-2

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Keywords

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