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

Symbiosis

Volumn 57, Issue 3, 2012, Pages 127-132

  Middlebrooks, Michael L ^a   Bell, Susan S ^a   Pierce, Sidney K ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Animal photosynthesis; Chlorophyll synthesis; Kleptoplasty; Sacoglossan

Indexed keywords

ALGA; CHLOROPHYLL; DIGESTION; KLEPTOPARASITISM; PHOTOSYNTHESIS; PLASTID; SLUG; STARVATION;

ALGAE; ANIMALIA; GASTROPODA; OPISTHOBRANCHIA;

EID: 84868197083     PISSN: 03345114     EISSN: 18787665     Source Type: Journal    
DOI: 10.1007/s13199-012-0187-x     Document Type: Article

References (37)

1. Clark KB, Jensen KR, Stirts HM (1990) Survey for functional kleptoplasty among West Atlantic Ascoglossa (=Sacoglossa) (Mollusca Opisthobranchia). Veliger 33(4):339-345
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 (Pubitemid 44893396)
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 (Pubitemid 46155608)
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
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
6. Gallop A, Bartrop J, Smith DC (1980) The biology of chloroplast acquisition by Elysia viridis. Proc R Soc Lond B 207:335-349
7. Gibson GD, Toews DP, Bleakney JS (1986) Oxygen production and consumption in the sacoglossan (=ascoglossan) Elysia chlorotica Gould. Veliger 28(4):397-400
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
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
10. Greene RW (1970) Symbiosis in sacoglossan opisthobranchs: functional capacity of symbiotic chloroplasts. Mar Biol 7(2):138-142
11. Greene RW, Muscatine L (1972) Symbiosis in sacoglossan opisthobranchs: photosynthetic products of animal-chloroplast associations. Mar Biol 14(3):253-259
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
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
14. Joyard J, Dorne AJ, Douce R (1987) Use of thermolysin to probe the cytosolic surface of the outer membrane from plastids. Methods Enzymol 148:195-206
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 59:95-104 (Pubitemid 24407365)
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
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):126-137 (Pubitemid 36784681)
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
19. Pierce SK, Curtis NE (2012) Cell biology of the chloroplast symbiosis in sacoglossan sea slugs. Int Rev Cell Molec Biol 293:123-148
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 (Pubitemid 36738200)
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):23-38
22. Pierce SK, Curtis NE, Hanten JJ, Boerner SL, Schwartz JA (2007) Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 43:57-64 (Pubitemid 350104468)
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
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 29:1549-1556
25. 14C- labeled microalgal photosynthetic pigments. J Planton Res 18:1867-1880
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):371-381 (Pubitemid 28278546)
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):225-238
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
29. Stoecker DK, Swanberg N, Tyler S (1989) Oceanic mixotrophic flatworms. Mar Ecol Prog Ser 58(1-2):41-51
30. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:312-346 (Pubitemid 46986328)
31. Taylor DL (1971) Photosynthesis of symbiotic chloroplasts in Tridachia crispata (Bergh). Comp Biochem Physiol 38(1A):233-236
32. Trench RK, Greene RW, Bystrom BG (1969) Chloroplasts as functional organelles in animal tissues. J Cell Biol 42(2):404-417
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):335-349
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
35. Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59(5):1069-1080. doi: 10.1093/jxb/erm328 (Pubitemid 351644644)
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
37. West HH (1979) Chloroplast symbiosis and development of the ascoglossan opisthobranch, Elysia chlorotica. (PhD thesis Northeastern Univ) pp 161