Laboratory culturing of Elysia chlorotica reveals a shift from transient to permanent kleptoplasty

Symbiosis

Volumn 58, Issue 1-3, 2012, Pages 221-232

  Pelletreau, Karen N ^a,b   Worful, Jared M ^a,c   Sarver, Kara E ^a,d   Rumpho, Mary E ^a,b  

^a UNIVERSITY OF MAINE   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c IMMUNOGEN INC   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Elysia chlorotica; Invertebrate development; Kleptoplasty; Symbiosis; Vaucheria litorea

Indexed keywords

ABUNDANCE; FITNESS; FOOD AVAILABILITY; FOOD CONSUMPTION; GASTROPOD; GREEN ALGA; HOST-SYMBIONT INTERACTION; LABORATORY METHOD; METAMORPHOSIS; PLASTID; SALTMARSH; STARVATION; SURVIVAL; SYMBIOSIS;

ALGAE; ANIMALIA; ELYSIA CHLOROTICA; INVERTEBRATA; VAUCHERIA; VAUCHERIA LITOREA; XANTHOPHYCEAE;

EID: 84874935715     PISSN: 03345114     EISSN: 18787665     Source Type: Journal    
DOI: 10.1007/s13199-012-0192-0     Document Type: Conference Paper

References (64)

1. Capo TR, Bardales AT, Gillette PR, Lara MR, Schmale MC, Serafy JE (2009) Larval growth, development, and survival of laboratory-reared Aplysia californica: effects of diet and veliger density. Comp Biochem Physiol C 149(2):215-223
2. Clark KB, Jensen KR, Strits HM (1990) Survey for functional kleptoplasty among west Atlantic Ascoglossa (Sacoglossa) (Mollusca: Opisthobranchia). Veliger 33:339-345
3. Davis GM, Mazurkiewicz M, Mandracchia M (1982) Spurwinkia - morphology, systematics, and ecology of a new genus of North American marshland Hydrobiidae (mollusca, gastropoda). Proc Acad Nat Sci Phila 134:143-177
4. de Negri A, de Negri G (1876) Ber Deut Chem Ges Berl 9:84
5. Devine SP, Pelletreau KN, Rumpho ME (2012) 16S rDNA-based metagenomic analysis of bacterial diversity associated with two populations of the kleptoplastic sea slug Elysia chlorotica and its algal prey Vaucheria litorea. Biol Bull 223(1):138-154
6. Evertsen J, Burghardt I, Johnsen G, Wägele H (2007) Retention of functional chloroplasts in some sacoglossans from the Indo-pacific and Mediterranean. Mar Biol 151:2159-2166
7. Fujita T, Matsushita M, Endo Y (2004) The lectin-complement pathway - its role in innate immunity and evolution. Immunol Rev 198:185-202
8. Gordon AH, Darcy Hart P, Young MR (1980) Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature 286(5768):79-80
9. Goren MB (1977) Phagocyte lysosomes - interactions with infectious agents, phagosomes, and experimental perturbations in function. Annu Rev Microbiol 31:507-533
10. 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 Physiol 124(1):331-342
11. Green BJ, Fox TC, Rumpho ME (2005) Stability of isolated algal chloroplasts that participate in a unique mollusc/kleptoplast association. Symbiosis 40(1):31-40
12. Gross J, Bhattacharya D, Pelletreau KN, Rumpho ME, Reyes-Prieto A (2012) Secondary and tertiary endosymbiosis and kleptoplasty. In: Bock R, Knoop V, (eds) Advances in photosynthesis and respiration - Genomics of chloroplasts and mitochondria. Springer Science+Business Media B.V., 35, pp 000-000, doi: 10.1007/978-94-007-2920-9-2
13. Händeler K, Grzymbowski YP, Krug PJ, Wägele H (2009) Functional chloroplasts in metazoan cells - a unique strategy in animal life. Front Zool 6:28
14. Harrigan JF, Alkon DL (1978) Laboratory cultivation of Haminoea solitaria (Say, 1822) and Elysia chlorotica (Gould, 1870). Veliger 21(2):299-305
15. Hart PDA (1979) Phagosome-lysosome fusion in macrophages: a hinge in the intracellular fate of ingested microorganisms. Front Biol 48:409-423
16. Hibino T, Loza-Coll M, Messier C, Majeske AJ, Cohen AH, Terwilliger DP, Buckley KM, Brockton V, Nair SV, Berney K, Fugmann SD, Anderson MK, Pancer Z, Cameron RA, Smith LC, Rast JP (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300(1):349-365
17. Hohman TC, McNeil PL, Muscatine L (1982) Phagosome-lysosome fusion inhibited by algal symbionts of Hydra viridis. J Cell Biol 94(1):56-63
18. Jones TC, Hirsch JG (1972) Interactions between Toxoplasma gondii and mammalian cells 2. Absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J Exp Med 136(5):1173-1194
19. Karakashian SJ, Rudzinska MA (1981) Inhibition of lysosomal fusion with symbiont-containing vacuoles in Paramecium bursaria. Exp Cell Res 131(2):387-393
20. Kawaguti S, Yamasu T (1965) Electron microscopy on the symbiosis between and elysioid gastropod and chloroplasts of a green alga. Biol J Okayama Univ 11:57-65
21. Kodama Y, Fujishima M (2010) Secondary symbiosis between Paramecium and Chlorella cells. Int Rev Cell Mol Biol 279:33-77
22. Kriegstein AR, Castellucci V, Kandel ER (1974) Metamorphosis of Aplysia californica in laboratory culture. Proc Natl Acad Sci USA 71(9):3654-3658
23. Krug PJ (1998) Poecilogony in an estuarine opisthobranch: planktotrophy, lecithotrophy, and mixed clutches in a population of the ascoglossan Alderia modesta. Mar Biol 132(3):483-494
24. Krug PJ (2007) Poecilogony and larval ecology in the gastropod genus Alderia. Am Malacol Bull 23(1-2):99-111
25. McFall-Ngai M, Nyholm SV, Castillo MG (2010) The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol 22(1):48-53
26. Messier-Solek C, Buckley KM, Rast JP (2010) Highly diversified innate receptor systems and new forms of animal immunity. Semin Immunol 22(1):39-47
27. Mondy WL, Pierce SK (2003) Apoptotic-like morphology is associated with annual synchronized death in kleptoplastic sea slugs (Elysia chlorotica). Invert Biol 122(2):126-137
28. Müjer 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. Proc Natl Acad Sci USA 93(22):12333-12338
29. Muscatine L, McNeil PL (1989) Endosymbiosis in Hydra and the evolution of internal defense systems. Am Zool 29(2):371-386
30. Nyholm SV, McFall-Ngai MJ (2004) The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2(8):632-642
31. Nyholm SV, Stewart JJ, Ruby EG, McFall-Ngai MJ (2009) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 11(2):483-493
32. Pelletreau KN, Bhattacharya D, Price DC, Worful JM, Moustafa A, Rumpho ME (2011) Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiol 155(4):1561-1565
33. Pethe K, Swenson DL, Alonso S, Anderson J, Wang C, Russell DG (2004) Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc Natl Acad Sci USA 101(37):13642-13647
34. Pierce SK, Curtis NE (2012) Cell biology of the chloroplast symbiosis in sacoglossan sea slugs. In: Jeon KW (ed) International review of cell and molecular biology, 293. Academic, Burlington, pp 123-148
35. Pierce SK, Biron RW, Rumpho ME (1996) Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol 199:2323-2330
36. 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. Biol Bull 197(1):1-6
37. Pierce SK, Massey SE, Hanten JJ, Curtis NE (2003) Horizontal transfer of functional nuclear genes between multicellular organisms. Biol Bull 204(3):237-240
38. Pierce SK, Curtis NE, Hanten JJ, Boerner SL, Schwartz JA (2007) Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 43(2):57-64
39. Pierce SK, Curtis NE, Schwartz JA (2009) Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49(3):121-131
40. Plaut I, Borut A, Spira ME (1995) Growth and metamorphosis of Aplysia oculifera larvae in laboratory culture. Mar Biol 122(3):425-430
41. Pluddemann A, Mukhopadhyay S, Gordon S (2011) Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry. Immunol Rev 240:11-24
42. Rast JP, Messier-Solek C (2008) Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biol Bull 214(3):274-283
43. Rast JP, Smith LC, Loza-Coll M, Hibino T, Litman GW (2006) Review - genomic insights into the immune system of the sea urchin. Science 314(5801):952-956
44. Rosenstiel P, Philipp ER, Schreiber S, Bosch TG (2009) Evolution and function of innate immune receptors - insights from marine invertebrates. J Innate Immun 1(4):291-300
45. Rowley AF, Powell A (2007) Invertebrate immune systems-specific, quasi-specific, or nonspecific? J Immunol 179(11):7209-7214
46. Rumpho ME, Summer EJ, Manhart JR (2000) Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol 123(1):29-38
47. 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(3-4):303-312
48. Rumpho ME, Dastoor FP, Manhart JR, Lee J (2006) The kleptoplast. In: Wise RR, Hoober JK (eds) Advances in photosynthesis and respiration: the structure and function of plastids. Springer, Dordrecht, pp 451-473
49. 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. Proc Natl Acad Sci USA 105(46):17867-17871
50. Rumpho ME, Pochareddy S, Worful JM, Summer EJ, Bhattacharya D, Pelletreau KN, Tyler MS, Lee J, Manhart JR, Soule KM (2009) Molecular characterization of the Calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. Mol Plant 2(6):1384-1396
51. Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D (2011) The making of a photosynthetic animal. J Exp Biol 214:303-311
52. Russell DG, Mwandumba HC, Rhoades EE (2002) Mycobacterium and the coat of many lipids. J Cell Biol 158(3):421-426
53. 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
54. Soule KM, Rumpho ME (2012) Light-regulated photosynthetic gene expression and phosphoribulokinase enzyme activity in the heterokont alga Vaucheria litorea (Xanthophyceae) and its symbiotic molluscan partner Elysia chlorotica (Gastropoda). J Phyc 48(2):373-383
55. Switzer-Dunlap M, Hadfield MG (1977) Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia). J Exp Mar Biol Ecol 29:245-261
56. Trench RK (1975) Of 'leaves that crawl': functional chloroplasts in animal cells. In: Jennings DH (ed) Symp Soc Exp Biol, Cambridge University Press, London, pp 229-265
57. 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
58. Trowbridge CD (2000) The missing links: larval and post-larval development of the ascoglossan opisthobranch Elysia viridis. J Mar Biol Assoc UK 80(6):1087-1094
59. Vergne I, Chua J, Singh SB, Deretic V (2004) Cell biology of Mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 20:367-394
60. West HH (1979) Chloroplast symbiosis and development of the ascoglossan opistobranch Elysia chlorotica. PhD thesis, Northeastern University, Boston, MA
61. West HH, Harrigan J (1979) Symbiosis and development in two populations of Elysia chlorotica. Am Zool 19(3):958
62. West HH, Harrigan JF, Pierce SK (1984) Hybridization of two populations of a marine opisthobranch with different developmental patterns. Veliger 26(3):199-206
63. Worful JM (2008) Elysia chlorotica (Gould, 1870): towards the development of a novel system for the elucidation of horizontal gene transfer, invertebrate developmental biology and secondary metabolites. M.S Thesis, University of Maine
64. Yamamoto YY, Yusa Y, Yamamoto S, Hirano Y, Hirano Y, Motomura T, Tanemura T, Obokata J (2009) Identification of photosynthetic sacoglossans from Japan. Encocytobiosis Cell Res 19:112-119