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Evidence against mutualism in an aeolid nudibranch associated with Symbiodiniaceae dinoflagellates

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Abstract

The symbiotic association with Symbiodiniaceae dinoflagellates has been more investigated for reef-building corals than for other metazoan taxa. Nudibranchs are relevant hosts as they present a wide variety of relationships with Symbiodiniaceae that range from predation to mutualistic association. The aeolid Berghia stephanieae is perhaps the best model for ecological studies in the mollusk-dinoflagellate association due to its hardiness, short life cycle and simple aquaculture protocols. However, it remains untested if B. stephanieae and Symbiodiniaceae actually engage in mutualism. Therefore, this study experimentally investigated the following aspects pertaining to the relationship between the two organisms: (i) Symbiodiniaceae retention time in the host tissue, (ii) effect of Symbodiniaceae presence in the prey item on host growth, and (iii) host capability to obtain free-living Symbiodiniaceae. Three experiments were performed: (i) monitoring of Symbiodiniaceae concentration in the cerata of starved B. stephanieae, (ii) offer of different-sized prey with and without symbionts and measuring B. stephanieae growth, and (iii) offer of free-living Symbiodiniaceae to B. stephanieae. Results show that the retention time (3–5 days) is much shorter than for many symbiont-associated nudibranchs. Berghia stephanieae growth is influenced by prey size, and apparently not affected by symbiont presence. Finally, this species is unable to obtain free-living Symbiodiniaceae. These results indicate that B. stephanieae does not meet criteria for a mutualistic relationship with Symbiodiniaceae, such as long-term retention and metabolite or favor exchange. This relationship may be in an evolutionary transitional stage, unlike the fully functional mutualism found in other organisms such as reef-building corals.

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References

  • Allemand D, Furla P, Benazet-Tambutte S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941

    CAS  Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Google Scholar 

  • Banger D (2011) Breeding Berghia Nudibranches – the best kept secret. CreateSpace Independent Publishing Platform

  • Burghardt I, Gosliner TM (2006) Phyllodesmium rudmani (Mollusca: Nudibranchia: Aeolidoidea), a new solar powered species from the Indo-West Pacific with data on its symbiosis with zooxanthellae. Zootaxa 1308:31–47

    Google Scholar 

  • Burghardt I, Wägele H (2004) A new solar powered species of the genus Phyllodesmium Ehrenberg, 1831 (Mollusca: Nudibranchia: Aeolidoidea) from Indonesia with analysis of its photosynthetic activity and notes on biology. Zootaxa 596(1):18

    Google Scholar 

  • Burghardt I, Wägele H (2014) The symbiosis between the 'solar-powered' nudibranch Melibe engeli Risbec, 1937 (Dendronotoidea) and Symbiodinium sp. (Dinophyceae). J Molluscan Stud 80:508–517

    Google Scholar 

  • Burghardt I, Evertsen J, Johnsen G, Wägele H (2005) Solar powered seaslugs - Mutualistic symbiosis of aeolid nudibranchia (Mollusca, Gastropoda, Opisthobranchia) with Symbiodinium. Symbiosis 38:227–250

    Google Scholar 

  • Burghardt I, Stemmer K, Wägele H (2008) Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca: Gastropoda), with analyses of long-term retention. Org Divers Evol 8:66–76

    Google Scholar 

  • Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J Exp Biol 215:3467–3477

    PubMed  PubMed Central  CAS  Google Scholar 

  • Carmona L, Pola M, Gosliner TM, Cervera JL (2013) A tale that morphology fails to tell: a molecular phylogeny of Aeolidiidae (Aeolidida, Nudibranchia, Gastropoda). PLoS One 8:e63000

    PubMed  PubMed Central  CAS  Google Scholar 

  • Carroll DJ, Kempf SC (1990) Laboratory culture of the aeolid nudibranch Berghia-verrucicornis (Mollusca, Opisthobranchia) - some aspects of its development and life-history. Biol Bull 179:243–253

    PubMed  CAS  Google 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 15:23–26

    Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate Symbiosis. Microbiol Mol Biol Rev 76:229–261

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dionísio G, Faleiro F, Rosa R (2017) Snails, slugs and cephalopods. In: Calado R, Olivotto I, Oliver MP, Holt GJ (eds) Marine ornamental species aquaculture. Wiley Online Library, pp 536–563

  • Fitt WK, Fisher CR, Trench RK (1986) Contribution of the symbiotic dinoflagellate Symbiodinium-microadriaticum to the nutrition, growth and survival of larval and juvenile tridacnid clams. Aquaculture 55:5–22

    Google Scholar 

  • Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19:1283–1293

    PubMed  CAS  Google Scholar 

  • Grant AJ, Remond M, People J, Hinde R (1997) Effects of host-tissue homogenate of the scleractinian coral Plesiastrea versipora on glycerol metabolism in isolated symbiotic dinoflagellates. Mar Biol 128:665–670

    CAS  Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    PubMed  CAS  Google Scholar 

  • Hillesland KL, Stahl DA (2010) Rapid evolution of stability and productivity at the origin of a microbial mutualism. P Natl Acad Sci USA 107:2124–2129

    CAS  Google Scholar 

  • Hoegh-Guldberg O, Hinde R (1986) Studies on a nudibranch that contains zooxanthellae .1. Photosynthesis, respiration and the translocation of newly fixed carbon by zooxanthellae in Pteraeolidia ianthina. Proc R Soc Ser B-Bio 228:493–509

    Google Scholar 

  • Hoegh-Guldberg O, Hinde R, Muscatine L (1986) Studies on a nudibranch that contains zooxanthellae .2. Contribution of zooxanthellae to animal respiration (czar) in Pteraeolidia ianthina with high and low-densities of zooxanthellae. Proc R Soc Ser B-Bio 228:511–521

    Google Scholar 

  • Kempf SC (1984) Symbiosis between the zooxanthella Symbiodinium (= Gymnodinium) microadriaticum (Freudenthal) and 4 species of nudibranchs. Biol Bull 166:110–126

    Google Scholar 

  • Kempf SC (1991) A primitive symbiosis between the aeolid nudibranch Berghia verrucicornis (A Costa, 1867) and a zooxanthella. J Molluscan Stud 57:75–85

    Google Scholar 

  • Klumpp DW, Bayne BL, Hawkins AJS (1992) Nutrition of the giant clam Tridacna gigas (L.). I. Contribution of filter feeding and photosynthates to respirations and growth. J Exp Mar Biol Ecol 155:105–122

    Google Scholar 

  • LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:136–134

    Google Scholar 

  • Leal MC, Nunes C, Alexandre D, da Silva TL, Reis A, Dinis MT, Calado R (2012a) Parental diets determine the embryonic fatty acid profile of the tropical nudibranch Aeolidiella stephanieae: the effect of eating bleached anemones. Mar Biol 159:1745–1751

    CAS  Google Scholar 

  • Leal MC, Nunes C, Engrola S, Dinis MT, Calado R (2012b) Optimization of monoclonal production of the glass anemone Aiptasia pallida (Agassiz in Verrill, 1864). Aquaculture 354:91–96

    Google Scholar 

  • Leggat W, Buck BH, Grice A, Yellowlees D (2003) The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host. Plant Cell Environ 26:1951–1961

    CAS  Google Scholar 

  • McFarland FK, Muller-Parker G (1993) Photosynthesis and retention of zooxanthellae and zoochlorellae within the aeolid nudibranch Aeolidia papillosa. Biol Bull 184:223–229

    PubMed  CAS  Google Scholar 

  • Melo Clavijo J, Donath A, Serôdio J, Christa G (2018) Polymorphic adaptations in metazoans to establish and maintain photosymbiosis. Biol Rev 93:2006–2020

    PubMed  Google Scholar 

  • Mies M, Braga F, Scozzafave MS, de Lemos DEL, Sumida PYG (2012) Early development, survival and growth rates of the giant clam Tridacna crocea (Bivalvia: Tridacnidae). Braz J Oceanogr 60:127–133

    Google Scholar 

  • Mies M, Sumida PYG, Rädecker N, Voolstra CR (2017a) Marine invertebrate larvae associated with Symbiodinium: a mutualism from the start? Front Ecol Evol 5:56

    Google Scholar 

  • Mies M, Voolstra CR, Castro CB, Pires DO, Calderon EN, Sumida PYG (2017b) Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae. R Soc Open Sci 4:170253

    PubMed  PubMed Central  CAS  Google Scholar 

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in coral reefs. In: Dubinsky Z (ed) Coral reefs: ecosystems of the world (25). Elsevier, Amsterdam, pp 75–87

    Google Scholar 

  • Norton JH, Shepherd MA, Long HM, Fitt WK (1992) The zooxanthellal tubular system in the giant clam. Biol Bull 183:503–506

    PubMed  CAS  Google Scholar 

  • Olivotto I, Planas M, Simoes N, Holt GJ, Avella MA, Calado R (2011) Advances in breeding and rearing marine ornamentals. J World Aquacult Soc 42:135–166

    Google Scholar 

  • Papina M, Meziane T, van Woesik R (2003) Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp Biochem Phys B 135:533–537

    CAS  Google Scholar 

  • Rudman WB (1981) The anatomy and biology of alcyonarian-feeding aeolid opisthobranch mollusks and their development of symbiosis with zooxanthellae. Zool J Linnean Soc 72:219–262

    Google Scholar 

  • Rudman WB (1991) Further-studies on the taxonomy and biology of the octocoral-feeding genus Phyllodesmium Ehrenberg, 1831 (Nudibranchia, Aeolidoidea). J Molluscan Stud 57:167–203

    Google Scholar 

  • Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts - Symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol 8:23–43

    Google Scholar 

  • Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci U S A 105:9256–9261

    PubMed  PubMed Central  CAS  Google Scholar 

  • Trench RK (1980) Uptake, retention and function of chloroplasts in animal cells. In: Schwemmler W, Schenk HEA (eds) Endocytobiology: endosymbiosis and cell biology, a synthesis of recent research. De Gruyter, Berlin, pp 703–727

    Google Scholar 

  • Valdés A (2005) A new species of Aeolidiella Bergh, 1867 (Mollusca: Nudibranchia: Aeolidiidae) from the Florida keys, USA. Veliger 47:218–223

    Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080

    PubMed  CAS  Google Scholar 

  • Wägele H (2004) Potential key characters in Opisthobranchia (Gastropoda, Mollusca) enhancing adaptive radiation. Org Divers Evol 4:175–188

    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, Raupach MJ, Burghardt I, Grzymbowski Y, Händeler K (2010) Solar powered seaslugs (Opisthobranchia, Gastropoda, Mollusca): incorporation of photosynthetic units: a key character enhancing radiation? In: Glaubrecht M (ed) Evolution in action. Springer. Heidelberg, Berlin, pp 263–282

    Google Scholar 

  • Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringe JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23:369–376

    PubMed  Google Scholar 

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Acknowledgements

We would like to thank Fundação de Pesquisas e Estudos Aquáticos (FUNDESPA) and Eco-Reef for providing infra-structure. We also thank two anonymous reviewers, G., Maurício Shimabukuro, Orlemir Carrerette, Linda Waters and Kenneth Halanych for insights and reviewing the paper, and Lucas Canela for helping during the experiments. The authors acknowledge FAPESP Grant 2017/04098-6.

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  1. Oceanographic Institute, University of São Paulo (IO-USP), Praça do Oceanográfico, 191 – Cidade Universitária, São Paulo, SP, 05508-120, Brazil

    Estela A. Monteiro, Arthur Z. Güth, Thomás N. S. Banha, Paulo Y. G. Sumida & Miguel Mies

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  1. Estela A. Monteiro
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  4. Paulo Y. G. Sumida
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Contributions

E.A.M., A.Z.G., P.Y.G.S. and M.M. designed the experiment, E.A.M. performed the experiment, P.Y.G.S. and M.M. contributed with infrastructure/material/technical support, E.A.M., A.Z.G. and T.N.S.B. analyzed the data and E.A.M., T.N.S.B. and M.M. wrote the manuscript.

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Correspondence to Estela A. Monteiro.

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Monteiro, E.A., Güth, A.Z., Banha, T.N.S. et al. Evidence against mutualism in an aeolid nudibranch associated with Symbiodiniaceae dinoflagellates. Symbiosis 79, 183–189 (2019). https://doi.org/10.1007/s13199-019-00632-4

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