Crawling leaves: Photosynthesis in sacoglossan sea slugs

Journal of Experimental Botany

Volumn 64, Issue 13, 2013, Pages 3999-4009

  Cruz, Sónia ^a   Calado, Ricardo ^a   Serôdio, João ^a   Cartaxana, Paulo ^b  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

Author keywords

Endosymbiosis; kleptoplasty; PAM fluorometry; photobiology; photoprotection; photosynthesis; sacoglossa; symbiosis.

Indexed keywords

ANIMAL; AUTOTROPHY; CHLOROPLAST; CLASSIFICATION; ENDOSYMBIOSIS; FLUOROMETRY; GASTROPOD; KLEPTOPLASTY; LIGHT; LIGHT PROTECTION; PAM FLUOROMETRY; PHOTOBIOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; RADIATION EXPOSURE; REVIEW; SACOGLOSSA; SYMBIOSIS; SYMBIOSIS.;

ENDOSYMBIOSIS; KLEPTOPLASTY; PAM FLUOROMETRY; PHOTOBIOLOGY; PHOTOPROTECTION; PHOTOSYNTHESIS; SACOGLOSSA; SYMBIOSIS.;

ANIMALS; AUTOTROPHIC PROCESSES; CHLOROPLASTS; FLUOROMETRY; GASTROPODA; LIGHT; PHOTOSYNTHESIS; SYMBIOSIS;

EID: 84886918465     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert197     Document Type: Review

References (89)

1. Baker NR, Oxborough K. 2004. Chlorophyll fluorescence as a probe of photosynthetic productivity. In: GC Papageorgious, Govindjee, eds, Chlorophyll a fluorescence: a signature of photosynthesis , vol. 19. Dordrecht, The Netherlands: Springer, pp 66-83.
2. Cartaxana P, Ruivo M, Hubas C, Davison I, Serôdio J, Jesus B. 2011. Physiological versus behavioral photoprotection in intertidal epipelic and epipsammic benthic diatom communities. Journal of Experimental Marine Biology and Ecology 405, 120-127.
3. Cartaxana P, Serôdio J. 2008. Inhibiting diatom motility: a new tool for the study of the photophysiology of intertidal microphytobenthic biofilms. Limnology and Oceanography: Methods 6, 466-476.
4. Chow WS. 1994. Photoprotection and photoinhibitory damage. Advances in Molecular and Cell Biology 10, 151-96.
5. Christa G, Wescott L, Schäberle TF, König GM, Wägele H. 2013. What remains after 2 months of starvation? Analysis of sequestered algae in a photosynthetic slug, Plakobranchus ocellatus (Sacoglossa, Opisthobranchia), by barcoding. Planta 237, 559-572.
6. Clark KB. 1994. Ascoglossan (=sacoglossan) molluscs in the Florida Keys: rare marine invertebrates at special risk. Bulletin of Marine Science 54, 900-916.
7. Clark KB, Busacca M. 1978. Feeding specificity and chloroplast retention in four tropical ascoglossa, with a discussion of the extent of chloroplast symbiosis and the evolution of the order. Journal of Molluscan Studies 44, 272-282.
8. Clark KB, Jensen KR, Stirts HM. 1990. Survey for functional kleptoplasty (chloroplast symbiosis) among West Atlantic Ascoglossa (=Sacoglossa) (Mollusca: Opisthobranchia). Veliger 33, 339-345.
9. Costa J, Giménez-Casalduero F, Melo R, Jesus B. 2012. Colour morphotypes of Elysia timida (Sacoglossa, Gastropoda) are determined by light acclimation in food algae. Aquatic Biology 17, 81-89.
10. Cruz S, Dionísio G, Rosa R, Calado R, Serôdio J. 2012. Anesthetizing solar-powered sea slugs for photobiological studies. The Biological Bulletin 223, 328-326.
11. Cruz S, Serôdio J. 2008. Relationship of rapid light curves of variable fluorescence to photoacclimation and non-photochemical quenching in a benthic diatom. Aquatic Botany 88, 256-264.
12. Curtis NE, Massey SE, Pierce SK. 2006. The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Invertebrate Biology 125, 336-345.
13. 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. Marine Biology 150, 797-806.
14. Demming-Adams B. 2003. Linking the xanthophyll cycle with thermal energy dissipation. Photosynthesis Research 76, 73-80.
15. Dionísio G, Rosa R, Leal MC, Cruz S, Brandão C, Calado G, Serôdio J, Calado R. Beauties and beasts: a portrait of sea slugs aquaculture. Aquaculture 408-409, 1-14.
16. Eberhard S, Finazzi G, Wollman FA. 2008. The dynamics of photosynthesis. Annual Review of Genetics 42, 463-515.
17. Edelman M, Mattoo AK. 2008. The D1 protein: past and future perspectives. In: B Demming-Adams, WW Adams III, A Mattoo, eds, Photoprotection, photoinhibition, gene regulation and environment , vol. 21. Dordrecht, The Netherlands: Springer, pp 23-38.
18. 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.
19. 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. Marine Biology 156, 847-859.
20. Gallop A, Bartrop J, Smith DC. 1980. The biology of chloroplast acquisition by Elysia viridis. Proceedings of the Royal Society B 207, 335-349.
21. Genty B, Briantais JM, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87-92.
22. Giménez-Casalduero F, Muniain C. 2006. Photosynthetic activity of the solar-powered lagoon mollusk Elysia timida (Risso, 1818) (Opisthobranchia: Sacoglossa). Symbiosis 41, 151-158.
23. Giménez-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. Journal of Experimental Marine Biology and Ecology 357, 181-187.
24. Giménez-Casalduero F, Muniain C, González-Wangüemert, Garrote-Moreno A. 2011. Elysia timida (Risso, 1818) three decades of research. Animal Biodiversity and Conservation 34, 217-227.
25. Goss R, Jakob T. 2010. Regulation and function of xanthophylls cycle-dependent photoprotection in algae. Photosynthesis Research 106, 102-122.
26. Green BJ, Li WY, Manhart JR, Fox TC, Summer EJ, 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 Physiology 124, 331-342.
27. Händeler K, Grzymbowski YP, Krug PJ, Wägele H. 2009. Functional chloroplasts in metazoan cells- A unique strategy in animal life. Frontiers in Zoology 6, 28-45.
28. Hanten JJ, Pierce SK. 2001. Synthesis of several light-harvesting complex I polypeptides is blocked by cycloheximide in symbiotic chloroplasts in the sea slug Elysia chlorotica (Gould): a case of horizontal gene transfer between alga and animal? The Biological Bulletin 201, 34-44.
29. Hawes CR. 1979. Ultrastructural aspects of the symbiosis between algal chloroplasts and Elysia viridis. New Phytologist 83, 445-450.
30. Hinde R, Smith DC. 1972. Persistence of functional chloroplast in Elysia viridis (Opistobranchia, Sacoglossa). Nature New Biology 239, 30-31.
31. Hinde R, Smith DC. 1975. The role of photosynthesis in the nutrition of the mollusc, Elysia viridis. Biological Journal of the Linnean Society 7, 161-171.
32. Horton P, Ruban AV, Walters RG. 1996. Regulation of light harvesting in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 655-684.
33. Jensen KR. 1980. A review of sacoglossan diets, with comparative notes on radular and buccal anatomy. Malacological Review 13, 55-77.
34. Jesus B, Ventura P, Calado G. 2010. Behaviour and a functional xanthophyll cycle enhance photo-regulation mechanisms in the solarpowered sea slug Elysia timida (Risso, 1818). Journal of Experimental Marine Biology and Ecology 395, 98-105.
35. Johnson MD. 2011. The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynthesis Research 107, 117-132.
36. Kao W-Y, Forseth IN. 1992. Diurnal leaf movement, chlorophyll fluorescence and carbon assimilation in soybean grown under different nitrogen and water availabilities. Plant, Cell and Environment 15, 703-710.
37. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M. 2002. Chloroplasts avoidance movement reduces photodamage in plants. Nature 420, 829-832.
38. Kawaguti S, Yamasu T. 1965. Electron microscopy on the symbiosis between and elysioid gastropod and chloroplasts of a green alga. Biological Journal of Okayama University 11, 57-65.
39. Klochkova TA, Han JW, Kim JH, Kim KY, Kim GH. 2010. Feeding specificity and photosynthetic activity of Korean sacoglossan mollusks. Algae 25, 217-227.
40. Klochkova TA, Han JW, Chah KH, Kim RW, Kim JH, Kim KY, Kim GH. 2013. Morphology, molecular phylogeny and photosynthetic activity of the sacoglossan mollusk, Elysia nigrocapitata, from Korea. Marine Biology 160, 155-168.
41. Maeda T, Hirose E, Chikaraishi Y, et al. 2012. Algivore or phototroph? Plakobranchus ocellatus (Gastropoda) continuously acquires kleptoplasts and nutrition from multiple algal species in nature. PLoS ONE 7, e42024.
42. Marín A, Ros J. 1992. Dynamics of a peculiar plant-herbivore relationship: the photosynthetic ascoglossan Elysia timida and the chlorophycean Acetabularia acetabulum. Marine Biology 112, 677-682.
43. Marín A, Ros J. 1993. Ultrastructual and ecological aspects of the development of chloroplast retention in the sacoglossan gastropod, Elysia timida. Journal of Molluscan Studies 59, 95-104.
44. Maxwell K, Johnson GL. 2000. Chlorophyll fluorescence- A practical guide. Journal of Experimental Botany 51, 659-668.
45. Middlebrooks ML, Pierce SK, Bell SS. 2012. Foraging behavior under starvation conditions is altered via photosynthesis by the marine gastropod, Elysia clarki. PLoS ONE 6(7), e22162.
46. Mujer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME. 1996. Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proceedings of the National Academy of Sciences, USA 93, 12333-12338.
47. Müller P, Li X-P, Niyogi KK. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558-1566.
48. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI. 2007. Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta 1767, 414-421.
49. Niyogi KK. 1999. Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50, 333-359.
50. Oxborough K. 2004. Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. Journal of Experimental Botany 55, 1195-1205.
51. Pelletreau KN, Bharracharya D, Price DC, Worful JM, Moustafa A, Rumpho ME. 2011. Update on sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiology 155, 1561-1565.
52. Pelletreau KN, Worful JM, Sarver KE, Rumpho ME. 2012. Laboratory culturing of Elysia chlorotica reveals a shift from transient to permanent kleptoplasty. Symbiosis 58, 221-232.
53. Pierce SK, Biron RW, Rumpho ME. 1996. Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. Journal of Experimental Biology 199, 2323-2330.
54. Pierce SK, Curtis NE. 2012. Cell biology of the chloroplast symbiosis in sacoglossan sea slugs. In: KW Jeon, ed, International review of cell and molecular biology , vol. 293. Burlington: Academic Press, pp 123-148.
55. 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.
56. Pierce SK, Curtis NE, Schwartz JA. 2009. Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49, 121-131.
57. Pierce SK, Fang X, Schwartz JA, Jiang X, Zhao W, Curtis NE, Kocot KM, Yang B, Wang J. 2012. Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Molecular Biology and Evolution 29, 1545-1556.
58. Pierce SK, Maugel TK, Rumpho ME, Hanten JJ, Mondy WL. 1999. Annual viral expression in a sea slug population: life cycle control and symbiotic chloroplast maintenance. The Biological Bulletin 197, 1-6.
59. Rahat M, Monselise EBI. 1979. Photobiology of the chloroplast hosting mollusk Elysia timida (Opistobranchia). Journal of Experimental Biology 79, 225-233.
60. Raven JA, Beardall J, Flynn KJ, Maberlyet SC. 2009. Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin's insectivorous plants. Journal of Experimental Botany 60, 3975-3987.
61. Raven JA, Walker DI, Jensen KR, Handley LL, Scrimgeour CM, McInroy SG. 2001. What fraction of the organic carbon in sacoglossans is obtained from photosynthesis by kleptoplastids? An investigation using the natural abundance of stable carbon isotopes. Marine Biology 138, 537-545.
62. Rumpho ME, Dastoor FP, Manhart JR, Lee J. 2007. The kleptoplast. In: RR Wise, JK Hoober, eds, Advances in photosynthesis and respiration-the structure and function of plastids , vol. 23. New York: Springer, pp 451-473.
63. Rumpho ME, Summer EJ, Green BJ, Fox TC, Manhart JR. 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.
64. Rumpho ME, Summer EJ, Manhart JR. 2000. Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiology 123, 29-38.
65. Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D. 2011. The making of a photosynthetic animal. Journal of Experimental Biology 214, 303-311.
66. Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug, Elysia chlorotica. Proceedings of the National Academy of Sciences, USA 105, 17867-17871.
67. Schmitt V, Wägele H. 2011. Behavioral adaptations in relation to long-term retention of endosymbiotic chloroplasts in the sea slug Elysia timida (Opisthobranchia, Sacoglossa). Thalassas 27, 225-238.
68. Schreiber U. 2004. Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: GC Papageorgious, Govindjee, eds, Chlorophyll a fluorescence: a signature of photosynthesis , vol. 19. Dordrecht, The Netherlands: Springer, pp 279-319.
69. Schreiber U, Gademann R, Ralph PJ, Larkum AWD. 1997. Assessment of photosynthetic performance of Prochloron in Lissoclinum patella in hospite by chlorophyll fluorescence measurements. Plant and Cell Physiology 38, 945-951.
70. Strasser RJ, Tsimilli-Michael M, Srivastava A. 2004. Analysis of the chlorophyll a fluorescence transient. In: GC Papageorgious, Govindjee, eds, Chlorophyll a fluorescence: a signature of photosynthesis , vol. 19. Dordrecht, The Netherlands: Springer, pp 321-362.
71. Serôdio J. 2004. Analysis of variable chlorophyll fluorescence in microphytobenthos assemblages: implications of the use of depthintegrated measurements. Aquatic Microbial Ecology 36, 137-152.
72. Serôdio J, Coelho H, Vieira S, Cruz S. 2006. Microphytobenthos vertical migratory photoresponse as characterised by light-response curves of surface biomass. Estuarine Coastal and Shelf Science 68, 547-556.
73. Serôdio J, Pereira S, Furtado J, Silva R, Coelho H, Calado R. 2010. In vivo quantification of kleptoplastic chlorophyll a content in the 'solar-powered' sea slug E. viridis using optical methods: spectral reflectance analysis and PAM fluorometry. Photochemical and Photobiological Studies 9, 68-77.
74. Serôdio J, Silva R, Ezequiel J, Calado R. 2011. Photobiology of the symbiotic acoel flatworm Symsagittifera roscoffensis: algal symbiont photoacclimation and host photobehaviour. Journal of the Marine Biological Association of the United Kingdom 91, 163-171.
75. Szabó I, Bergantino E, Giacometti GM. 2005. Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO Reports 6, 629-634.
76. Trench RK. 1975. Of 'leaves that crawl'; functional chloroplasts in animal cells. Symposia of the Society for Experimental Biology 29, 229-265.
77. Trench RK, Boyle JE, Smith DC. 1973. The association between chloroplasts of Codium fragile and the mollusc Elysia viridis II: chloroplast ultrastructure and photosynthetic carbon fixation in Elysia viridis. Proceedings of the Royal Society B 184, 63-81.
78. Trench RK, Ohlhorst S. 1976. The stability of chloroplasts from siphonaceous algae in symbiosis with sacoglossan molluscs. New Phytologist 76, 99-109.
79. Trowbridge CD. 2000. The missing links: larval and post-larval development of the ascoglossan opisthobranch Elysia viridis. Journal of the Marine Biological Association of the United Kingdom 80, 1087-1094.
80. Ventura P, Calado G, Jesus B. 2013. Photosynthetic efficiency and kleptoplast pigment diversity in the sea slug Thuridilla hopei (Vérany, 1853). Journal of Experimental Marine Biology and Ecology 441, 105-109.
81. Vieira S, Calado R, Coelho H, Serôdio J. 2009. Effects of light exposure on the retention of kleptoplastic photosynthetic activity in the sacoglossan mollusc Elysia viridis. Marine Biology 156, 1007-1020.
82. Wägele H. 2004. Potential key characters in Opistobranchia (Gastropoda, Mollusca) enhancing adaptive radiation. Organisms, Diversity and Evolution 4, 175-188.
83. Wägele H, Deusch O, Händeler K, et al. 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. Molecular Biology and Evolution 28, 699-706.
84. 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 and Evolution 1, 193-210.
85. Weaver S, Clark KB. 1981. Light intensity preference of five ascoglossan (=sacoglossan) molluscs (Gastropoda: Opisthobranchia): a comparison of chloroplast-symbiotic and aposymbiotic species. Marine Behavior and Physiology 7, 297-306.
86. West HH. 1979. Chloroplast symbiosis and development of the ascoglossan opisthobranch Elysia chlorotica. PhD thesis. Boston: Northeastern University.
87. West HH, Harrigan JF, Pierce SK. 1984. Hybridization of two populations of a marine opisthobranch with different developmental patterns. Veliger 26, 199-206.
88. White AJ, Critchley C. 1999. Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynthesis Research 59, 63-72.
89. Yamamoto S, Hirano YM, Hirano YJ, Trowbridge CD, Akimoto A, Sakai A, Yusa Y. 2013. Effects of photosynthesis on the survival and weight retention of two kleptoplastic sacoglossan opisthobranchs. Journal of the Marine Biological Association of the United Kingdom 98, 209-215.