Symbiosis

, Volume 57, Issue 3, pp 127–132

The kleptoplastic sea slug Elysia clarki prolongs photosynthesis by synthesizing chlorophyll a and b

  • Michael L. Middlebrooks
  • Susan S. Bell
  • Sidney K. Pierce
Article

Abstract

Several species of kleptoplastic, sacoglossan sea slug photosynthesize using chloroplasts sequestered inside their digestive cells from algal food sources. However, sequestered chloroplasts alone are not sufficient for months-long, continuous photosynthesis and maintenance of the chloroplasts in absence of the algal nucleus. Some type of plastid maintenance mechanism must be present to help sustain photosynthetic activity in the long term kleptoplastic species, such as Elysia clarki. We demonstrate that E. clarki starved for 2 weeks are able to synthesize chlorophylls, but that slugs starved for 14 weeks no longer synthesize chlorophyll. The subsidence of chlorophyll synthesis is coincident with the cessation of photosynthesis by the starved slugs, but it is not yet known if the cessation of pigment synthesis is the cause or some other aspect of plastid degradation produces a loss of synthetic ability.

Keywords

Sacoglossan Kleptoplasty Chlorophyll synthesis Animal photosynthesis 

References

  1. Clark KB, Jensen KR, Stirts HM (1990) Survey for functional kleptoplasty among West Atlantic Ascoglossa (=Sacoglossa) (Mollusca Opisthobranchia). Veliger 33(4):339–345Google Scholar
  2. Curtis NE, Massey SE, Pierce SK (2006) The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Invertebr Biol 125(4):336–345. doi:10.1111/j.1744-7410.2006.00065.x CrossRefGoogle Scholar
  3. Curtis NE, Pierce SK, Massey SE, Schwartz JA, Maugel TK (2007) Newly metamorphosed Elysia clarki juveniles feed on and sequester chloroplasts from algal species different from those utilized by adult slugs. Mar Biol 150:797–806. doi:10.1007/s00227-006-0398-x CrossRefGoogle Scholar
  4. Evertsen J, Johnsen G (2009) In vivo and in vitro differences in chloroplast functionality in the two north Atlantic sacoglossans (Gastropoda, Opisthobranchia) Placida dendritica and Elysia viridis. Mar Biol 156(5):847–859. doi:10.1007/s00227-009-1128-y CrossRefGoogle Scholar
  5. Furuya K, Hayashi M, Yabushita Y (1998) HPLC determination of phytoplankton pigments using N, N-dimethylformamide. J Oceanogra 54(2):199–203. doi:10.1007/bf02751695 CrossRefGoogle Scholar
  6. Gallop A, Bartrop J, Smith DC (1980) The biology of chloroplast acquisition by Elysia viridis. Proc R Soc Lond B 207:335–349CrossRefGoogle Scholar
  7. Gibson GD, Toews DP, Bleakney JS (1986) Oxygen production and consumption in the sacoglossan (=ascoglossan) Elysia chlorotica Gould. Veliger 28(4):397–400Google Scholar
  8. Gimènez-Casalduero F, Muniain C (2008) The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818): (Sacoglossa: Opisthobranchia) during periods of food shortage. J Exp Mar Biol Ecol 357(2):181–187. doi:10.1016/j.jembe.2008.01.020 CrossRefGoogle Scholar
  9. Green BJ, Li W-y, Manhart JR, Fox TC, Kennedy RA, Pierce SK, Rumpho ME (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 Physiol 124:331–342. doi:10.1104/pp.124.1.331 Google Scholar
  10. Greene RW (1970) Symbiosis in sacoglossan opisthobranchs: functional capacity of symbiotic chloroplasts. Mar Biol 7(2):138–142CrossRefGoogle Scholar
  11. Greene RW, Muscatine L (1972) Symbiosis in sacoglossan opisthobranchs: photosynthetic products of animal-chloroplast associations. Mar Biol 14(3):253–259Google Scholar
  12. Händeler K, Grzymbowski YP, Krug PJ, Wägele H (2009) Functional chloroplasts in metazoan cells — a unique evolutionary strategy in animal life. Front Zool 6:28. doi:10.1186/1742-9994-6-28 PubMedCrossRefGoogle Scholar
  13. Jesus B, Ventura P, Calado G (2010) Behaviour and a functional xanthophyll cycle enhance photo-regulation mechanisms in the solar-powered sea slug Elysia timida (Risso, 1818). J Exp Mar Biol Ecol 395(1–2):98–105. doi:10.1016/j.jembe.2010.08.021 CrossRefGoogle Scholar
  14. Joyard J, Dorne AJ, Douce R (1987) Use of thermolysin to probe the cytosolic surface of the outer membrane from plastids. Methods Enzymol 148:195–206CrossRefGoogle Scholar
  15. Marin A, Ros J (1993) Ultrastructural and ecological aspects of the developement of chloroplast retention in the sacoglossan gastropod Elysia timida. J Molluscan Stud 59:95–104CrossRefGoogle Scholar
  16. Middlebrooks ML, Pierce SK, Bell SS (2011) Foraging behavior under starvation conditions is altered via photosynthesis by the marine gastropod, Elysia clarki. PLoS One 6(7):e22162. doi:10.1371/journal.pone.0022162 PubMedCrossRefGoogle Scholar
  17. Mondy WL, Pierce SK (2003) Apoptotic-like morphology is associated with annual synchronized death in kleptoplastic sea slugs (Elysia chlorotica). Invertebr Biol 122(2):126–137CrossRefGoogle Scholar
  18. Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328(5978):624–627. doi:10.1126/science.1187113 PubMedCrossRefGoogle Scholar
  19. Pierce SK, Curtis NE (2012) Cell biology of the chloroplast symbiosis in sacoglossan sea slugs. Int Rev Cell Molec Biol 293:123–148CrossRefGoogle Scholar
  20. Pierce SK, Massey SE, Hanten JJ, Curtis NE (2003) Horizontal transfer of functional nuclear genes between multicellular organisms. Biol Bull 204(3):237–240. doi:10.2307/1543594 PubMedCrossRefGoogle Scholar
  21. Pierce SK, Curtis NE, Massey SE, Bass AL, Karl SA, Finney CM (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 Res 26(1):23–38Google Scholar
  22. Pierce SK, Curtis NE, Hanten JJ, Boerner SL, Schwartz JA (2007) Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 43:57–64Google Scholar
  23. Pierce SK, Curtis NE, Schwartz JA (2009) Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49(3):121–131. doi:10.1007/s13199-009-0044-8 CrossRefGoogle Scholar
  24. Pierce SK, Fang X, Schwartz J, Jiang X, Zhao W, Curtis NE (2012) Transcriptomic evidence for the expression of horizontally transferred nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Mol Biol Evol 29:1549–1556CrossRefGoogle Scholar
  25. Pinckney JL, Millie DF, Howe KE, Paerl HW, Hurley JP (1996) Flow scintillation counting of 14C- labeled microalgal photosynthetic pigments. J Planton Res 18:1867–1880CrossRefGoogle Scholar
  26. Pinckney JL, Paerl HW, Harrington MB, Howe KE (1998) Annual cycles of phytoplankton community structure and bloom dynamics in the Neuse River Estuary, North Carolina. Mar Biol 131(2):371–381CrossRefGoogle Scholar
  27. Schmitt V, Wägele H (2011) Behavioral adaptations in relation to long-term retention of endosymbiotic chloroplasts in the sea slug Elysia timida (Opistobranchia, Sacoglossa). Thalassas 27(2):225–238Google Scholar
  28. Schwartz JA, Curtis NE, Pierce SK (2010) Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evol Biol 37(1):29–37. doi:10.1007/s11692-010-9079-2 CrossRefGoogle Scholar
  29. Stoecker DK, Swanberg N, Tyler S (1989) Oceanic mixotrophic flatworms. Mar Ecol Prog Ser 58(1–2):41–51CrossRefGoogle Scholar
  30. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:312–346CrossRefGoogle Scholar
  31. Taylor DL (1971) Photosynthesis of symbiotic chloroplasts in Tridachia crispata (Bergh). Comp Biochem Physiol 38(1A):233–236CrossRefGoogle Scholar
  32. Trench RK, Greene RW, Bystrom BG (1969) Chloroplasts as functional organelles in animal tissues. J Cell Biol 42(2):404–417PubMedCrossRefGoogle Scholar
  33. Trench RK, Trench ME, Muscatine L (1972) Symbiotic chloroplasts; their photosynthetic products and contribution to mucus synthesis in two marine slugs. Biol Bull 142(2):335–349PubMedCrossRefGoogle Scholar
  34. Trench RK, Boyle JE, Smith DC (1973) Association between chloroplasts of Codium fragile and mollusk Elysia viridis. 2. Chloroplast ultrastructure and photosynthetic carbon fixation in Elysia viridis. Proc R Soc Lond B 184(1074):63–81. doi:10.1098/rspb.1973.0031 CrossRefGoogle Scholar
  35. Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59(5):1069–1080. doi:10.1093/jxb/erm328 PubMedCrossRefGoogle Scholar
  36. Wägele H, Deusch O, Händeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould SB, Dagan T, Klussmann-Kolb A, Martin W (2011) Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Mol Biol Evol 28(1):699–706. doi:10.1093/molbev/msq239 PubMedCrossRefGoogle Scholar
  37. West HH (1979) Chloroplast symbiosis and development of the ascoglossan opisthobranch, Elysia chlorotica. (PhD thesis Northeastern Univ) pp 161Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Michael L. Middlebrooks
    • 1
  • Susan S. Bell
    • 1
  • Sidney K. Pierce
    • 1
  1. 1.Department of Integrative BiologyUniversity of South FloridaTampaUSA

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