Skip to main content
SpringerLink
Log in

Chlorophyll a synthesis by an animal using transferred algal nuclear genes

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Chlorophyll synthesis is an ongoing requirement for photosynthesis and a ubiquitous, diagnostic characteristic of plants and algae amongst eukaryotes. However, we have discovered that chlorophyll a (Chla) is synthesized in the symbiotic chloroplasts of the sea slug, Elysia chlorotica, for at least 6 months after the slugs have been deprived of the algal source of the plastids, Vaucheria litorea. In addition, using transcriptome analysis and PCR with genomic DNA, we found 4 expressed genes for nuclear-encoded enzymes of the Chla synthesis pathway that have been horizontally transferred from the alga to the genomic DNA of the sea slug. These findings demonstrate the first discovery of Chla production in an animal using transferred nuclear genes from its algal food.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Curtis, N.E., Massey, S.E., and Pierce, S.K. 2006. The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Journal of Invertebrate Biology 125: 336–345.

    Article  Google Scholar 

  • Eberhard, S., Finazzi, G., and Wollman, F.-A. 2008. The dynamics of photosynthesis. Annual Review of Genetics 42: 463–515.

    Article  CAS  PubMed  Google Scholar 

  • Evertsen, J., Burghardt, I., Johnsen, G., and Wagele, H. 2007. Retention of functional chloroplasts in some sacoglossan from the Indo-Pacific and Mediterranean. Marine Biology 151: 2159–2166.

    Article  Google Scholar 

  • Gast, R.J., Moran, D.M., Dennett, M.R., and Caron, D.A. 2007. Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environmental Microbiology 9: 39–45.

    Article  CAS  PubMed  Google Scholar 

  • Graves, D.A., Gibson, M.A., and Bleakney, J.S. 1979. The digestive diverticula of Alderia modesta and Elysia chlorotica (Opisthobranchia : Sacoglossa). Veliger 21: 415–422.

    Google Scholar 

  • Green, B.J., Li, W.-Y., Manhart, J.R., Fox, T.C., Summer, E.J., Kennedy, R.A., Pierce, S.K., and Rumpho, M.E. 2000. Molluscalgal 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 

  • Hanten, J.J. and Pierce, S.K. 2001. Synthesis of several lightharvesting complex I polypeptides is blocked by cycloheximide in symbiotic chloroplasts in the sea slug, Elysia chlorotica (Gould): A case for horizontal gene transfer between alga and animal? Biological Bulletin 201: 33–44.

    Article  Google Scholar 

  • Johnson, M.D., Oldach, D., Delwiche, C.F., and Stoecker, D.K. 2007. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445: 426–428.

    Article  CAS  PubMed  Google Scholar 

  • Llewellyn, C.A, Mantoura, R.F.C., and Brereton, R.G. 1990. Products of chlorophyll photodegradation -1 Detection and separation. Photochemistry and Photobiology 52: 1037–1041.

    Article  CAS  Google Scholar 

  • McLean, N. 1976. Phagocytosis of chloroplasts in Placida dendritica (Gastropoda: Sacoglossa). Journal of Experimental Zoology 197: 321–330.

    Article  Google Scholar 

  • Mondy, W.L. and Pierce, S.K. 2003. Apoptotic-like morphology is associated with the annual synchronized death of a population of kleptoplastic sea slugs (Elysia chlorotica). Journal of Invertebrate Biology 122: 126–137.

    Google Scholar 

  • Nayar, S., Goh, B.P.L., and Chou, L.M. 2003. Interference of chlorophyll a in liquid scintillation counting of phytoplankton productivity samples by the 14C technique. Estuarine and Coastal Shelf Science 56: 957–960.

    Article  CAS  Google Scholar 

  • Obornik, M. and Green, B.R. 2005. Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Molecular Biology and Evolution 22: 2343–2353.

    Article  CAS  PubMed  Google Scholar 

  • Owen, G. 1966. Digestion. In: Physiology of Mollusca II. Wilbur, K.M. and Yonge, C.M., eds. Academic Press, NY, pp. 53–96.

    Google Scholar 

  • Pierce, S.K., Biron, R.W., and 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 

  • Pierce, S.K., Curtis, N.E., Hanten, J.J., Boerner, S.L., and Schwartz, J.A. 2007. Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 43: 57–64.

    CAS  Google Scholar 

  • Pierce, S.K., Curtis, N.E., Massey, S.E., Bass, A.L., Karl, S.A., and Finney, C. 2006. A morphological and molecular comparison between Elysia crispata and a new species of kleptoplastic sacoglossan sea slug (Gastropoda: Opisthobranchia) from the Florida Keys USA. Molluscan Research 26: 23–38.

    CAS  Google Scholar 

  • Pierce, S.K., Maugel, T.K., Rumpho, M.E., Hanten, J.J., and 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 

  • Pinckney, J.L., Millie, D.F., Howe, K.E., Paerl, H.W., and Hurley, J.P. 1996. Flow scintillation counting of 14C-labeled microalgal photosynthetic pigments. Journal of Plankton Research 18: 1867–1880.

    Article  CAS  Google Scholar 

  • Pinckney, J.L., Paerl, H.W., Harrington, M.B., and Howe, K.E. 1998. Annual cycles of phytoplankton community-structure and bloom dynamics in the Neuse River Estuary, North Carolina. Marine Biology 131: 371–381.

    Article  Google Scholar 

  • Reith, M. 1995. Molecular biology of rhodophyte and chromophyte plastids. Annual Review of Plant Physiology and Molecular Biology 46: 549–575.

    Article  CAS  Google Scholar 

  • Riper, D.M., Owens, T.G., and Falkowski, P.G. 1979. Chlorophyll turnover in Skeletonema costatum, a marine plankton diatom. Plant Physiology 64: 49–54.

    Article  CAS  PubMed  Google Scholar 

  • Rumpho, M.E., Summer, E.J., Green, B.J., Fox, T.C., and 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 

  • Rumpho, M.E., Worful, J.M., Lee, J., Kannan, K., Tyler, M.S., Bhattacharya, D., Moustafa, A., and Manhart, J.R. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proceedings of the National Academy of Science, USA 105: 17867–17871.

    Article  CAS  Google Scholar 

  • Schwartz, J.A., Curtis, N.E., and Pierce, S.K. Transcriptome analysis reveals several horizontally transferred algal nuclear genes in the genome of the sea slug Elysia chlorotica. Journal of Molecular Evolution (submitted).

  • Tanaka, R. and Tanaka, A. 2007. Tetrapyrrole biosynthesis in higher plants. Annual Review of Plant Biology 58: 321–346.

    Article  CAS  PubMed  Google Scholar 

  • Wamsley, J. and Adamson, H. 1994. Chlorophyll turnover in etiolated greening barley transferred to darkness: Isotopic (1-14C glutamic acid) evidence of dark chlorophyll synthesis in the absence of chlorophyll accumulation. Physiologia Plantarum 93: 435–444.

    Google Scholar 

  • West, H.H., Harrigan, J., and Pierce, S.K. 1984. Hybridization of two populations of a marine opisthobranch with different developmental patterns. Veliger 26: 199–206.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Integrative Biology, SCA 110, University of South Florida, 4202 E. Fowler Ave., Tampa, FL, 33620, USA

    Sidney K. Pierce, Nicholas E. Curtis & Julie A. Schwartz

Authors
  1. Sidney K. Pierce
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicholas E. Curtis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie A. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sidney K. Pierce.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pierce, S.K., Curtis, N.E. & Schwartz, J.A. Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49, 121–131 (2009). https://doi.org/10.1007/s13199-009-0044-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-009-0044-8

Keywords

Search

Navigation