The ability to incorporate functional plastids by the sea slug Elysia viridis is governed by its food source
Functional kleptoplasty in sacoglossan sea slugs is among the most curious photosynthetic associations known. One member of these marine molluscs, Elysia viridis, is known to incorporate plastids from a variety of different algae food sources, but with apparently different outcomes and differences in the time span of the retention of functional kleptoplasts. While it was previously shown that kleptoplasts that stem from Codium tomentosum are kept functional for several weeks (long-term retention, LtR), those that stem from Bryopsis hypnoides or Cladophora rupestris are thought to be of limited use regarding photosynthetic capacity (short-term retention, StR). This is important, because it touches upon the popular yet controversial question of how important photosynthesis is for the thriving of these slugs. The aim of the present study was to determine to what degree the plastid source determines retention time. We, therefore, compared E. viridis feeding on either Cladophora sp. or B. hypnoides. We show that kleptoplasts of B. hypnoides incorporate 14CO2, but with rapidly declining efficiency throughout the first week of starvation, while the plastids of Cladophora sp. are, surprisingly, not incorporated to begin with. The radulae of the different samples showed adjustment to the food source, and when feeding on Cladophora sp., E. viridis survived under laboratory conditions under both starvation and non-starvation conditions. Our results demonstrate that (i) the ability to incorporate plastids by E. viridis differs between the food sources B. hypnoides and Cladophora sp., and (ii) photosynthetic active kleptoplasts are not an inevitable requirement for survival.
Funding through the DAAD (P.R.I.M.E.) and FCT to GC (SFRH/BPD/109892/2015), DFG to S.B.G. (GO1825/4-1), and through the ERC to Prof. William F. Martin (ERC 666053) is gratefully acknowledged. For financial support, thanks are due to Centre for Environmental and Marine Studies (UID/AMB/50017), FCT/Ministry of Science and Education through national funds, and the co-funding by European Fund For Regional Development, within the PT2020 Partnership Agreement and Compete 2020.
CR, SBG, JS and GC planned the experiments, which were conducted by CR, AGMT and GC. CR, SBG and GC wrote the manuscript, whose final version was approved by all authors. We thank Steffen Köhler (CAi, HHU) for imaging of the slugs and for his help with SEM imaging, and Marion Nissen (CAi, HHU) for her help with the TEM.
Compliance with ethical standards
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Conflict of interest
The authors declare no competing interests.
- Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689. https://doi.org/10.1146/annurev.ecolsys.34.011802.132417 CrossRefGoogle Scholar
- Burns JA, Zhang H, Hill E, Kim E, Kerney R (2017) Transcriptome analysis illuminates the nature of the intracellular interaction in a vertebrate-algal symbiosis. eLife Sci 6:e22054. https://doi.org/10.7554/elife.22054
- Casalduero FG, Muniain C (2006) Photosynthetic activity of the solar-powered lagoon mollusc Elysia timida (Risso, 1818) (Opisthobranchia: Sacoglossa). Symbiosis 41:151–158Google Scholar
- Christa G, Wescott L, Schäberle TF, König GM, Wägele H (2013b) What remains after 2 months of starvation? Analysis of sequestered algae in a photosynthetic slug, Plakobranchus ocellatus (Sacoglossa, Opisthobranchia), by barcoding. Planta 237(2):559–572. https://doi.org/10.1007/s00425-012-1788-6 CrossRefPubMedGoogle Scholar
- Christa G, Händeler K, Kück P, Vleugels M, Franken J, Karmeinski D, Wägele H (2015) Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda). Org Divers Evol 15(1):23–36. https://doi.org/10.1007/s13127-014-0189-z CrossRefGoogle Scholar
- Cueto M, D’Croz L, Maté JL, San-Martín A, Darias J (2005) Elysiapyrones from Elysia diomedea. Do such metabolites evidence an enzymatically assisted electrocyclization cascade for the biosynthesis of their bicyclo [4.2. 0] octane core? Org Lett 7(3):415–418. https://doi.org/10.1021/ol0477428 CrossRefPubMedGoogle Scholar
- Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Springer, Boston. https://doi.org/10.1007/978-1-4615-8714-9_3
- Hinde R (1978) The metabolism of photosynthetically fixed carbon by isolated chloroplasts from Codium fragile (Chlorophyta: Siphonales) and by Elysia viridis (Mollusca: Sacoglossa). Biol J Linn Soc 10(3):329–342. https://doi.org/10.1111/j.1095-8312.1978.tb00019.x CrossRefGoogle Scholar
- Hinde R, Smith D (1975) The role of photosynthesis in the nutrition of the mollusc Elysia viridis. Biol J Linn Soc 7(2):161–171. https://doi.org/10.1111/j.1095-8312.1975.tb00738.x CrossRefGoogle Scholar
- Jensen KR (1993) Morphological adaptations and plasticity of radular teeth of the Sacoglossa (=Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biol J Linn Soc 48(2):135–155. https://doi.org/10.1111/j.1095-8312.1993.tb00883.x CrossRefGoogle Scholar
- Jerschabek Laetz EM, Wägele H (2017) Chloroplast digestion and the development of functional kleptoplasty in juvenile Elysia timida (Risso, 1818) as compared to short-term and non-chloroplast-retaining sacoglossan slugs. PLoS One 12(10):e0182910. https://doi.org/10.1371/journal.pone.0182910 CrossRefPubMedGoogle Scholar
- Karasov WH, Martínez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, PrincetonGoogle Scholar
- 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. Mar Biol 138(3):537–545. https://doi.org/10.1007/s002270000488 CrossRefGoogle Scholar
- 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 Elysia viridis using optical methods: spectral reflectance analysis and PAM fluorometry. Photochem Photobiol Sci 9(1):68–77. https://doi.org/10.1039/B9PP00058E CrossRefPubMedGoogle Scholar
- Trench R, Boyle JE, Smith D (1973) 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(1074):63–81. https://doi.org/10.1098/rspb.1973.0031 CrossRefGoogle Scholar
- Trowbridge CD, Todd CD (2001) Host-plant change in marine specialist herbivores: ascoglossan sea slugs on introduced macroalgae. Ecol Monogr 71(2):219–243. https://doi.org/10.1890/0012-9615(2001)071[0219:HPCIMS]2.0.CO;2 CrossRefGoogle Scholar
- Wägele H, Martin WF (2013) Endosymbioses in sacoglossan sea slugs: plastid-bearing animals that keep photosynthetic organelles without borrowing genes. In: Löffelhardt W (ed) Endosymbiosis. Springer, Vienna, pp 291–324. https://doi.org/10.1007/978-3-7091-1303-5_14