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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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.
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.
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.
Eberhard, S., Finazzi, G., & Wollman, F. A. (2008). The dynamics of photosynthesis. Annual Review of Genetics, 42, 463–515.
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.
Gould, S. B., Waller, R. F., & McFadden, G. I. (2008). Plastid Evolution. Annual Review of Plant Biology, 59, 491–517.
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.
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.
Kleine, T., Voigt, C., & Leister, D. (2009). Plastid signalling to the nucleus: Messengers still lost in the mists? Trends in Genetics, 25, 185–192.
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.
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.
Masuda, T., & Fujita, Y. (2008). Regulation and evolution of chlorophyll metabolism. Photochemical & Photobiological Sciences, 7, 1131–1149.
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.
Pesaresi, P., Schneider, A., Kleine, T., & Leister, D. (2007). Interorganellar communication. Current Opinion in Plant Biology, 10, 600–606.
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.
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.
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.
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.
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.
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.
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.
Tanaka, R., & Tanaka, A. (2007). Tetrapyrrole biosynthesis in higher plants. Annual Review of Plant Biology, 58, 321–346.
Trench, R. K. (1969). Chloroplasts as functional organelles in animal tissues. Nature, 222, 1071–1072.
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.
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.
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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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
- Horizontal gene transfer
- Transcriptome analysis
- Chloroplast endosymbiosis
- Vaucheria litorea
- Elysia chlorotica