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Endosymbioses in Sacoglossan Seaslugs: Plastid-Bearing Animals that Keep Photosynthetic Organelles Without Borrowing Genes

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Endosymbiosis

Abstract

In this chapter, we summarize our knowledge on photosynthesis properties in the enigmatic gastropod group Sacoglossa. Members of this group are able to sequester chloroplasts from their food algae and store them for weeks and months in order to use them in a similar way as plants do.

Only four to five sacoglossan species are able to perform photosynthesis for months, others are less effective or are not able at all. The processes involved are not clear, but we show by this chapter that many factors contribute to the developing of a photosynthetic seaslug. These include extrinsic (environment, origin and properties of the nutrition and the plastids) and intrinsic factors (behaviour, physiological and anatomical properties). Maintenance of plastids is not enhanced by a horizontal gene transfer (HGT) from the algal genome into the slug genome, as was hypothesized for many years. We outline here the questions that now have to be asked and the research that has to be done to understand the factors that actually contribute to this unique metazoan phenomenon, which is not understood at all.

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References

  • Agardh CA (1823) Species algarum rite cognitae, cum synonymis, differentiis specificis et descriptionibus succinctis. Volumen primum pars posterior. ex officina Berlingiana, Lundae, pp 399–531

    Google Scholar 

  • Agardh CA (1873) Till algernes systematik. Nya bidrag. Lunds Universitets Års-Skrift. Afd Mathematik Naturvetenskap 9:1–71

    Google Scholar 

  • Agosin M, Repetto Y (1963) Studies on the metabolism of Echinococcus granulosus* – VII. Reactions of the tricarboxylic acid cycle in E. granulosus scolices. Comp Biochem Physiol 8:245–261

    CAS  Google Scholar 

  • Alder J, Hancock A (1843) Notice on a British species of Calliopaea d’Orbigny, and on four new species of Eolis with observations on the development and structure of the nudibranchiate Mollusca. Ann Mag Nat Hist 12:233–238

    Google Scholar 

  • Alder H, Hancock A (1862) Descriptions of a new genus and some new species of naked Mollusca. Ann Mag Nat Hist 10:261–265

    Google Scholar 

  • Baba K (1955) Opisthobranchia of Sagami Bay, supplement. Iwanami Shoten, Tokyo, p 59

    Google Scholar 

  • Brandley BK (1981) Ultrastructure of the envelope of Codium australicum (Silva) chloroplasts in the alga and after acquisition by Elysia maoria (Powell). New Phytol 89:679–686

    Google Scholar 

  • Brandley BK (1984) Aspects of the ecology and physiology of Elysia cf. furvacauda (Mollusca: Sacoglossa). Bull Mar Sci 34:207–219

    Google Scholar 

  • Burn RF (1958) Further Victorian Opisthobranchia. J Malacol Soc Aust 2:20–36

    Google Scholar 

  • Carmona L, Malaquias MAE, Gosliner TM, Pola M, Cervera JL (2011) Amphi-Atlantic distributitions and cryptic species in sacoglossan sea slugs. J Molluscan Stud 77:401–412

    Google Scholar 

  • Clark KB, Bussacca M (1978) Feeding specifity and chloroplast retention in four tropical Ascoglossa, with a discussion of the extent of chloroplast symbiosis and the evolution of the order. J Molluscan Stud 44:272–282

    Google Scholar 

  • Clark KB, Jensen KR, Stirts HM, Fermin C (1981) Chloroplast symbiosis in a non-Elysiid mollusc, Costasiella lilianae Marcus (Hermaeidae: Ascoglossa (= Sacoglossa)): effects of temperature, light intensity, and starvation on carbon fixation rate. Biol Bull 160:42–54

    Google Scholar 

  • Clark KB, Jensen KR, Stirts HM (1990) Survey for functional kleptoplasty among West Atlantic Ascoglossa (= Sacoglossa) (Mollusca: Opisthobranchia). Veliger 33:339–345

    Google Scholar 

  • Curtis NE, Massey SE, Schwartz JA, Maugel TK, Pierce SK (2005) The intracellular, functional chloroplasts in adult sea slugs (Elysia crispata) come from several algal species, and are also different from those in juvenile slugs. Microsc Microanal 11:1194–1195

    PubMed  Google Scholar 

  • Curtis NE, Massey SE, Pierce SK (2006) The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Invert Biol 125:336–345

    Google Scholar 

  • de Lamarck JBPA (1813) Sur les polypiers empâtés. Ann Mus Hist Nat, Paris 20:294–312, 370–386, 432–458

    Google Scholar 

  • De Negri A, De Negri G (1876) Bericht A. und G. De Negri (Gass. chim.). Ber Deut Chem Gesell 9:84

    Google Scholar 

  • Decaisne J (1842) Mémoire sur les corallines ou polypiers calcifères [la seconde partie du “Essais sur une classification des algues et des polypiers calcifères de Lamourous”]. Ann Sci Nat, Botanique, Sec Sér 18:96–128

    Google Scholar 

  • Di Marzo V, Marín A, Vardaro RR, De Petrocellis L, Villani G, Cimino G (1993) Histological and biochemical bases of defense mechanisms in four species of Polybranchioidea ascoglossan molluscs. Mar Biol 117:367–380

    Google Scholar 

  • Dinapoli A, Klussmann-Kolb A (2010) The long way to diversity – phylogeny and evolution of the Heterobranchia (Mollusca: Gastropoda). Mol Phylogenet Evol 55:60–76

    PubMed  Google Scholar 

  • Edmunds M (1963) Berthelinia caribbea n.sp., a bivalved gastropod from the Western Atlantic. Zool J Linn Soc 44:731–739

    Google Scholar 

  • Er M (1961) Opisthobranch mollusks from California. Veliger 3(Suppl):1–85

    Google Scholar 

  • Er M, Ev M (1967) American opisthobranch molluscs Part I, tropical American Opisthobranchs. Stud Trop Oceanogr Miami 6:1–256

    Google Scholar 

  • Evertsen J (2006) Retention of photosynthetic chloroplasts in five sacoglossans (Mollusca: Opisthobranchia) from the Houtman Abrolhos Islands. Rec West Aust Mus Suppl 69:133–135

    Google Scholar 

  • 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 156:847–859

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Gavagnin M, Marín A, Mollo E, Crispino A, Villani G, Cimino G (1994) Secondary metabolites from Mediterranean Elysioidea: origin and biological role. Comp Biochem Physiol 108B:107–115

    CAS  Google Scholar 

  • Gavagnin M, Mollo E, Montanaro D, Ortea J, Cimino G (2000) Chemical studies of Caribbean sacoglossans: dietary relationships with green algae and ecological implications. J Chem Ecol 26:1563–1578

    CAS  Google Scholar 

  • Giles KL, Sarafis V (1972) Chloroplast survival and division in vitro. Nat New Biol 236:56–58

    PubMed  CAS  Google Scholar 

  • 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. J Exp Mar Biol Ecol 357:181–187

    Google Scholar 

  • Gould AA (1870) Report on the Invertebrata of Massachusetts. Second edition, comprising the Mollusca. Wright and Potter, Boston, p 524

    Google Scholar 

  • Gould SB, Waller RR, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517

    PubMed  CAS  Google Scholar 

  • Grant BR, Borowitzka MA (1984a) Changes in structure of isolated chloroplasts of Codium fragile and Caulerpa filiformis in response to osmotic shock and detergent treatment. Protoplasma 120:155–164

    Google Scholar 

  • Grant BR, Borowitzka MA (1984b) The chloroplasts of giant-celled and coenocytic algae: biochemistry and structure. Bot Rev 50:267–307

    Google Scholar 

  • Graves DA, Gibson MA, Bleakney JS (1979) The digestive diverticula of Alderia modesta and Elysia chlorotica. Veliger 21:415–422

    Google Scholar 

  • Green BJ, Li W-Y, 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 124:331–342

    PubMed  CAS  Google Scholar 

  • Green BJ, Fox TC, Rumpho ME (2005) Stability of isolated algal chloroplasts that participate in a unique mollusc/kleptoplast association. Symbiosis 40:31–40

    Google Scholar 

  • Greene RW (1970) Symbiosis in sacoglossan opisthobranchs: functional capacity of symbiotic chloroplasts. Mar Biol 7:138–142

    CAS  Google Scholar 

  • Guiry MD, Guiry GM (2012) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; searched on 12 Feb 2012

  • Händeler K, Wägele H (2007) Preliminary study on molecular phylogeny of Sacoglossa and a compilation of their food organisms. Bonn Zool Beitr 3(4):231–254

    Google Scholar 

  • Händeler K, Grzymbowski Y, Krug JP, Wägele H (2009) Functional chloroplasts in metazoan cells – a unique evolutionary strategy in animal life. Front Zool 6:28

    PubMed  Google Scholar 

  • Händeler K, Wägele H, Wahrmund U, Rüdinger M, Knoop V (2010) Slugs’ last meals: molecular identification of sequestered chloroplasts from different algal origins in Sacoglossa (Opisthobranchia, Gastropoda). Mol Ecol Res 10:968–978

    Google Scholar 

  • Hanten JJ, Pierce SK (2001) Synthesis of several light-harvesting complex I polypeptides is blocked by cycloheximide in symbiotic chloroplast in the sea slug, Elysia chlorotica (Gould): a case for horizontal gene transfer between alga and animal? Biol Bull 201:34–44

    PubMed  CAS  Google Scholar 

  • Hariot P (1889) Mission Scientifique du Cap Horn. 1882–188.3 Botanique I. Algues. Gauthier-Villars et fils, Paris, pp 3–109

    Google Scholar 

  • van Hasselt JC (1824) In: Férussac A. Extrait d’une lettre du Dr. J.C. van Hasselt au Prof. van Swinderen sur mollusques de Java (traduit de l’Allgem. konst en letterbode, 1824, nos. 2,3,4) Tjuringe (ile Java) le 25 Mai 1823 (1). Bull Sci Nat Geol 3:237–248

    Google Scholar 

  • Hawes CR (1979) Ultrastructural aspects of the symbiosis between algal chloroplasts and Elysia viridis. New Phytol 83:445–450

    Google Scholar 

  • Hawes CR, Cobb AH (1980) The effects of starvation on the symbiotic chloroplasts in Elysia viridis: a fine structural study. New Phytol 84:375–379

    Google Scholar 

  • Hinde R, Smith DC (1972) Persistence of functional chloroplasts in Elysia viridis (Opisthobranchia, Sacoglossa). Nat New Biol 239:30–31

    PubMed  CAS  Google Scholar 

  • Hinde R, Smith DC (1974) “Chloroplast symbiosis” and the extent to which it occurs in Sacoglossa (Gastropoda: Mollusca). Biol J Linn Soc 6:349–356

    Google Scholar 

  • Hinde R, Smith DC (1975) The role of photosynthesis in the nutrition of the mollusc Elysia viridis. Biol J Linn Soc 7:161–171

    Google Scholar 

  • Hirose E (2005) Digestive system of the Sacoglossan Plakobranchus ocellatus (Gastropoda: Opisthobranchia): light- and electron-microscopic observations with remarks on chloroplast retention. Zoolog Sci 22:905–916

    PubMed  Google Scholar 

  • Ireland C, Scheuer PJ (1979) Photosynthetic marine mollusks: in vivo 14C incorporation into metabolites of the sacoglossan Placobranchus ocellatus. Science 205:922–923

    PubMed  CAS  Google Scholar 

  • Jensen KR (1980) A review of sacoglossan diets, with comparative notes on radular and buccal anatomy. Malac Rev 13:55–77

    Google Scholar 

  • Jensen KR (1987) Effect of starvation on copulatory activity of Ercolania nigra (Lemche, 1935) (Mollusca, Opisthobranchia, Ascoglossa). Mar Behav Physiol 13:89–97

    Google Scholar 

  • Jensen KR (1993a) Evolution of buccal apparatus and diet radiation in the Sacoglossa (Opisthobranchia). Boll Malacol 29:147–172

    Google Scholar 

  • Jensen KR (1993b) Morphological adaptations and plasticity of radular teeth of the Sacoglossa (=Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biol J Linn Soc 48:135–155

    Google Scholar 

  • Jensen KR (1994) Behavioural adaptations and diet specificity of sacoglossan opisthobranchs. Ethol Ecol Evol 6:87–101

    Google Scholar 

  • 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 395:98–105

    CAS  Google Scholar 

  • Johnson MD (2011) Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J Eukaryot Microb 58:185–195

    Google Scholar 

  • Jörger KM, Stöger I, Kano Y, Fukuda H, Knebelsberger T, Schrödl M (2011) On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evol Biol 10:323

    Google Scholar 

  • Kawaguti S, Yamasu T (1965) Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts of a green alga. Biol J Okayama Univ 11:57–65

    Google Scholar 

  • Klochkova TA, Han JW, Kim J-H, Kim KY, Kim GH (2010) Feeding specifity and photosynthetic activity of Korean sacoglossan mollusks. Algae 25:217–227

    Google Scholar 

  • Koike K, Sekiguchi H, Kobiyama A, Takishita K, Kawachi M, Koike K, Ogata T (2005) A novel type of kleptoplastidy in Dinophysis (Dinophyceae): presence of haptophyte-type plastid in Dinophysis mitra. Protist 156:225–237

    PubMed  CAS  Google Scholar 

  • Lamouroux JVF (1816) Histoire des polypiers coralligènes flexibles, vulgairement nommés zoophytes. F. Poisson, Caen, pp 1–560

    Google Scholar 

  • Lee JJ (2006) Algal symbiosis in larger foraminifera. Symbiosis 42:63–75

    Google Scholar 

  • Lovén SL (1844) Om nordiska hafs-mollusker. Kongl Vetensk Acad Handl 1:48–53

    Google Scholar 

  • Maeda T, Kajita T, Maruyama T, Hirano Y (2010) Molecular phylogeny of the Sacoglossa, with a discussion of gain and loss of kleptoplasty in the evolution of the group. Biol Bull 219:17–26

    PubMed  CAS  Google Scholar 

  • Maggs CA, Hommersand MH (1993) Seaweeds of the British Isles, vol 1, Rhodophyta. Part 3A. Ceramiales. HMSO, London, pp 1–444

    Google Scholar 

  • Marín A, Ros J (1989) The chloroplast-animal association in four Iberian sacoglossan opisthobranchs: Elysia timida, Elysia translucens, Thuridilla hopei, and Bosellia mimetica. Sci Mar 53:429–440

    Google Scholar 

  • Marín A, Ros J (1992) Dynamics of a peculiar plant-herbivore relationship: the photosynthetic ascoglossan Elysia timida and the chlorophycean Acetabularia acetabulum. Mar Biol 112:677–682

    Google Scholar 

  • Marín A, Ros J (1993) Ultrastructural and ecological aspects of the development of chloroplast retention in the sacoglossan gastropod Elysia timida. J Molluscan Stud 59:95–104

    Google Scholar 

  • Marín A, Ros J (2004) Chemical defenses in sacoglossan opisthobranchs: taxonomic trends and evolutive implications. Sci Mar 68:227–241

    Google Scholar 

  • Martin W, Cerff R (1986) Prokaryotic features of a nucleus encoded enzyme: cDNA sequences for chloroplast and cytosolyic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba). Eur J Biochem 159:323–331

    PubMed  CAS  Google Scholar 

  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17

    PubMed  CAS  Google Scholar 

  • Martin W, Schnarrenberger C (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 32:1–18

    PubMed  CAS  Google Scholar 

  • Martin W, Brinkmann H, Savona C, Cerff R (1993) Evidence for a chimaeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90:8692–8696

    PubMed  CAS  Google Scholar 

  • Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393:162–165

    PubMed  CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    PubMed  CAS  Google Scholar 

  • McLean N (1976) Phagocytosis of chloroplasts in Placida dendritica (Gastropoda: Sacoglossa). J Exp Zool 197:321–330

    Google Scholar 

  • Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralbl 25:593–604 [English translation in Martin W, Kowallik KV (1999) Eur J Phycol 34: 287–295]

    Google Scholar 

  • 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

    Google Scholar 

  • Monselise EBI, Rahat M (1980) Photobiology of Elysia timida (Mollusca: Opisthobranchia): observations in the sea. Isr J Zool 29:125–128

    Google Scholar 

  • Montagu G (1804) Description of several marine animals found on the south coast of Devonshire. Trans Linn Soc 11:1–26

    Google Scholar 

  • Montagu G (1815) An account of some new and rare British shells and animals. Trans Linn Soc Lond 11:179–204

    Google Scholar 

  • Mørch OAL (1863) Contributions a la faune malacologique des Antilles Danoises. J Conchol 11:21–43

    Google Scholar 

  • 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. Proc Natl Acad Sci USA 93:12333–12338

    PubMed  CAS  Google Scholar 

  • Müller OF (1774) Vermium terredtrium et fluviatilium, vol 2. Havniae & Lipsiae

    Google Scholar 

  • Muscatine L, Pool RR, Trench RK (1975) Symbiosis of algae and invertebrates: aspects of the symbiont surface and the host-symbiont interface. Trans Am Microsc Soc 94:450–469

    PubMed  CAS  Google Scholar 

  • Pelletreau KN, Bhattacharya D, Price DC, Worful JM, Moustafa A, Rumpho ME (2011) Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiol 155:1561–1565

    PubMed  CAS  Google Scholar 

  • Pierce SK, Biron RW, Rumpho ME (1996) Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol 199:2323–2330

    PubMed  CAS  Google Scholar 

  • Pierce SK, Massey SE, Hanten JJ, Curtis NE (2003) Horizontal transfer of functional nuclear genes between multicellular organisms. Biol Bull 204:237–240

    PubMed  Google Scholar 

  • 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. Moll Res 26:23–38

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Pierce SK, Curtis NE, Schwartz JA (2009) Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49:121–131

    CAS  Google Scholar 

  • Pierce SK, Fang X, Schwartz JA, Jian X, Zhao W, Curtis NE, Kocot K, Yang B, Wang J (2012) Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug Elysia chlorotica. Mol Biol Evol 29:1545–1556

    PubMed  CAS  Google Scholar 

  • Pruvot-Fol A (1957) Diagnose dune Elysie peut-être nouvelle de la Méditerranée. Bull Mus Nat d’Hist Natur 29:337–339

    Google Scholar 

  • Rahat M, Monselise EBI (1979) Photobiology of the chloroplast hosting mollusc Elysia timida (Opisthobranchia). J Exp Biol 79:225–233

    Google Scholar 

  • Risso A (1818) Mémoire sur quelques gastéropodes nouveaux, nudibranches et tectibranches observés dans la Mer de Nice. J Phys Chim Hist Nat Arts 87:368–377

    Google Scholar 

  • Ros J, Marín A (1990) Adaptive advantages of the “symbiosis” between algal chloroplasts and sacoglossan molluscs. Oecol Aquat 10:271–298

    Google Scholar 

  • Rudman WB (2012) Seaslugforum. http://www.seaslugforum.net/; World-wide electronic publication, Australian Museum; searched on 12 Feb 2012

  • Rumpho ME, Summer EJ, Manhart JR (2000) Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol 123:29–38

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Rumpho ME, Dastoor FP, Manhart JR, Lee J (2006) The kleptoplast. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, The Netherlands, pp 451–473

    Google Scholar 

  • Rumpho ME, Worful JM, Lee J, Kannan K, Tylor 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 105:17867–17871

    PubMed  CAS  Google Scholar 

  • Rumpho ME, Pochareddy S, Worful JM, Summer EJ, Bhattacharya D, Pelletreau KN, Tylor 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 2:1384–1396

    PubMed  CAS  Google Scholar 

  • Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D (2011) The making of a photosynthetic animal. J Exp Biol 214:303–311

    PubMed  Google Scholar 

  • Schimper AFW (1883) Über die Entwicklung der Chlorophyllkörner und Farbkörper. Bot Zeitung 41:105–114

    Google Scholar 

  • 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

    Google Scholar 

  • Schöttler U, Bennet EM (1991) Annelids. In: Bryant C (ed) Metazoan life without oxygen. Chapman and Hall, London, UK, pp 165–185

    Google Scholar 

  • Schwartz JA, Curtis NE, Pierce SK (2010) Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evol Biol 37:29–37

    Google Scholar 

  • Silva PC (1952) A review of nomenclatural conservation in the algae from the point of view of the type method. Univ Calif Publ Bot 25:241–323

    Google Scholar 

  • Simroth H (1895) Neuere Arbeiten über Opisthobranchien. Zool Centralbl 2:513–515

    Google Scholar 

  • Stoecker DK, Johnson MD, de Vargas C, Not F (2009) Acquired phototrophy in aquatic protists. Aquat Microb Ecol 57:279–310

    Google Scholar 

  • Swennen C (2011) Large mangrove-dwelling Elysia species in Asia, with descriptions of two new species (Gastropoda: Opisthobranchia: Sacoglossa). Raffl Bull Zool 59:29–37

    Google Scholar 

  • Taylor DL (1968) Chloroplasts as symbiotic organelles in the digestive gland of Elysia viridis (Gastropoda: Opisthobranchia). J Mar Biol Assoc UK 48:1–15

    Google Scholar 

  • Taylor DL (1971) Symbiosis between the chloroplasts of Griffithsia flosculosa (Rhodophyta) and Hermaea bifida (Gastropoda: Opisthobranchia). Pubbl Staz Zool Nap 39:116–120

    Google Scholar 

  • Teugels B, Bouillon S, Veuger B, Middelburg JJ, Koedam N (2008) Kleptoplasts mediate nitrogen acquisition in the sea slug Elysia viridis. Aquat Biol 4:15–21

    Google Scholar 

  • Thompson TE, Jarman GM (1989) Nutrition of Tridachia crispata (Mörch) (Sacoglossa). J Molluscan Stud 55:239–244

    Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    PubMed  CAS  Google Scholar 

  • Trench RK (1969) Chloroplasts as functional endysmbionts in the Mollusc Tridachia crispata (Bergh), (Opisthobranchia, Sacoglossa). Nature 222:1071–1072

    Google Scholar 

  • Trench RK (1973) Further studies on the mucoploysaccharide secreted by the pedal gland of the marine slug Tridachia crispata (Opisthobranchia, Sacoglossa). Bull Mar Sci 23:299–312

    CAS  Google Scholar 

  • Trench RK (1975) Of “leaves that crawl”, functional chloroplasts in animal cells. Symp Soc Exp Biol 29:229–265

    PubMed  CAS  Google Scholar 

  • Trench RK, Smith DC (1970) Synthesis of pigment in symbiotic chloroplasts. Nature 227:196–197

    PubMed  CAS  Google Scholar 

  • Trench RK, Greene RW, Bystrom BG (1969) Chloroplasts as functional organelles in animal tissues. J Cell Biol 42:404–417

    PubMed  CAS  Google Scholar 

  • Trench ME, Trench RK, Muscatine L (1970) Utilization of photosynthetic products of symbiotic chloroplasts in mucus synthesis by Placobranchus ianthobapsus (Gould), Opisthobranchia, Sacoglossa. Comp Biochem Physiol 37:113–117

    CAS  Google Scholar 

  • Trench RK, Boyle JE, Smith DC (1973a) The association between chloroplasts of Codium fragile and the mollusc Elysia viridis I. Characteristics of isolated Codium chloroplasts. Proc R Soc Lond B Biol Sci 184:51–61

    CAS  Google Scholar 

  • Trench RK, Boyle JE, Smith DC (1973b) The association between chloroplasts of Codium fragile and the mollusc Elysia viridis II. Chloroplast ultrastructure and photosynthetic carbon fixation in E. viridis. Proc R Soc Lond B Biol Sci 184:63–81

    CAS  Google Scholar 

  • Trench RK, Boyle JE, Smith DC (1974) The association between chloroplasts of Codium fragile and the mollusc Elysia viridis III. Movement of photosynthetically fixed 14C in tissues of intact living E. viridis and in Tridachia crispata. Proc R Soc Lond B Biol Sci 185:453–464

    CAS  Google Scholar 

  • Verany M (1853) Catalogue des Mollusques cephalopodes, pteropodes, Gasteropodes nudibranches, etc.... des environs de Nice. J Conchiol 4:375–392

    Google Scholar 

  • Vieira S, Calado G, Coelho H, Serôdio J (2009) Effects of light exposure on the retention of kleptoplastic photosynthetic activity in the sacoglossan mollusc Elysia viridis. Mar Biol 156:1007–1020

    CAS  Google Scholar 

  • Wägele H, Johnsen G (2001) Observations on the histology and photosynthetic performance of “solar-powered” opisthobranchs (Mollusca, Gastropoda; Opisthobranchia) containing symbiotic chloroplasts or zooxanthellae. Org Divers Evol 1:193–210

    Google Scholar 

  • Wägele H, Klussmann-Kolb A (2005) Opisthobranchia (Mollusca, Gastropoda) – more than just slimy slugs. Shell reduction and its implications on defence and foraging. Front Zool 2:1–18

    Google Scholar 

  • Wägele H, Klussmann-Kolb A, Vonnemann V, Medina M (2008) Heterobranchia I, the Opisthobranchia. In: Ponder W, Lindbergh W (eds) Phylogeny and evolution of the Mollusca. University of California Press, Berkeley, CA, pp 383–406

    Google Scholar 

  • Wägele H, Raupach MJ, Burghardt I, Grzymbowski Y, Händeler K (2010a) Solar powered seaslugs (Opisthobranchia, Gastropoda, Mollusca): incorporation of photosynthetic units: a key character enhancing radiation? In: Glaubrecht M (ed) Evolution in action. Springer, Berlin, pp 263–283

    Google Scholar 

  • Wägele H, Stemmer K, Burghardt I, Händeler K (2010b) Two new sacoglossan sea slug species (Opisthobranchia, Gastropoda): Ercolania annelyleorum sp. nov. (Limapontioidea) and Elysia asbecki sp. nov. (Plakobranchoidea) with notes on anatomy, histology and biology. Zootaxa 2676:1–28

    Google Scholar 

  • 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 28:699–706

    PubMed  Google Scholar 

  • Waugh GR, Clark KB (1986) Seasonal and geographic variation in chlorophyll level of Elysia tuca (Ascoglossa: Opisthobranchia). Mar Biol 92:483–487

    Google Scholar 

  • Weaver S, Clark KB (1981) Light intensity and color preferences of five ascoglossan (=sacoglossan) molluscs (Gastropoda: Opisthobranchia): a comparison of chloroplast-symbiotic and aposymbiotic species. Mar Behav Physiol 7:297–306

    Google Scholar 

  • Yamamoto YY, Yusa Y, Yamamoto S, Hirano Y, Hirano Y, Motomura T, Tanemura T, Obokata J (2009) Identification of photosynthetic sacoglossans from Japan. Endocyt Cell Res 19:112–119

    Google Scholar 

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Acknowledgements

We wish to thank Katharina Händeler (Bonn), Gregor Christa (Bonn), Valerie Schmitt (Düsseldorf), Rainer Martin (Ulm) and Elise Lätz (Bonn) for discussions. The DFG (German Science Foundation) (Wa 618/8, Wa 618/12, SFBTr1) and the ERC (Networkorigins) provided financial support. Information on taxonomic status of algal species were taken from AlgaeBase (Guiry and Guiry 2012) and on sacoglossan species from the Seaslugforum (Rudman 2012) (http://www.seaslugforum.net/; searched on 12 February 2012). We follow the conventions of the International Code of Zoological/Botanical Nomenclature and include names of the authors who described the mentioned species and additionally cite the original work.

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Wägele, H., Martin, W.F. (2014). Endosymbioses in Sacoglossan Seaslugs: Plastid-Bearing Animals that Keep Photosynthetic Organelles Without Borrowing Genes. In: Löffelhardt, W. (eds) Endosymbiosis. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1303-5_14

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