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The Chimerical and Multifaceted Marine Acoel Symsagittifera

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The Chimerical and Multifaceted Marine Acoel Symsagittifera The chimerical and multifaceted marine acoel Symsagittifera roscoffensis: from photosymbiosis to brain regeneration Xavier Bailly, Laurent Laguerre, Gaëlle Correc, Sam Dupont, Thomas Kurth, Anja Pfannkuchen, Rolf Entzeroth, Ian Probert, Serge Vinogradov, Christophe Lechauve, et al. To cite this version: Xavier Bailly, Laurent Laguerre, Gaëlle Correc, Sam Dupont, Thomas Kurth, et al.. The chimeri- cal and multifaceted marine acoel Symsagittifera roscoffensis: from photosymbiosis to brain regen- eration. Frontiers in Microbiology, Frontiers Media, 2014, 5, pp.498. 10.3389/fmicb.2014.00498. hal-01100635 HAL Id: hal-01100635 https://hal.sorbonne-universite.fr/hal-01100635 Submitted on 6 Jan 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEW ARTICLE published: 02 October 2014 doi: 10.3389/fmicb.2014.00498 The chimerical and multifaceted marine acoel Symsagittifera roscoffensis: from photosymbiosis to brain regeneration Xavier Bailly 1*, Laurent Laguerre 1, Gaëlle Correc 2, Sam Dupont 3, Thomas Kurth 4, Anja Pfannkuchen 4, Rolf Entzeroth 5, Ian Probert 6, Serge Vinogradov 7, Christophe Lechauve 8, Marie-José Garet-Delmas 9, Heinrich Reichert 10 and Volker Hartenstein 11 1 Université Pierre et Marie Curie -CNRS, FR2424, Functional Exploration in Marine Model Organisms - Centre de Ressources Biologiques Marines, Station Biologique de Roscoff, Roscoff, France 2 Université Pierre et Marie Curie -CNRS, UMR 7139, Marine Plants and Biomolecules, Station Biologique de Roscoff, Roscoff, France 3 Department of Biological and Environmental Sciences, The Sven Lovén Centre for Marine Sciences – Kristineberg, University of Gothenburg – Fiskebäckskil, Sweden 4 TU Dresden, DFG-Research Center for Regenerative Therapies Dresden, Dresden, Germany 5 Institute of Zoology, Technical University Dresden, Dresden, Germany 6 Université Pierre et Marie Curie -CNRS, FR2424, RCC (Roscoff Culture Collection) - Centre de Ressources Biologiques Marines, Station Biologique de Roscoff, Roscoff, France 7 Department of Biochemistry and Molecular Biology, Wayne State University School of Medicine, Detroit, France 8 INSERM, UMR S 968, CNRS/Université Pierre et Marie Curie - Institut de la Vision/Centre Hospitalier National d’Ophtalmologie des Quinze-Vingts, Paris, France 9 CNRS UMR 7144 and Université Pierre and Marie Curie, EPEP - Evolution of Protists and Pelagic Ecosystems, Station Biologique de Roscoff, Roscoff, France 10 Biozentrum, University of Basel, Basel, Switzerland 11 Department of Molecular Cell and Developmental Biology, University of California, Los Angeles, CA, USA Edited by: A remarkable example of biological engineering is the capability of some marine animals to Ute Hentschel, University of take advantage of photosynthesis by hosting symbiotic algae. This capacity, referred to as Wuerzburg, Germany photosymbiosis, is based on structural and functional complexes that involve two distantly Reviewed by: unrelated organisms. These stable photosymbiotic associations between metazoans and Mary E. Rumpho, University of Connecticut, USA photosynthetic protists play fundamental roles in marine ecology as exemplified by Angela Elizabeth Douglas, Cornell reef communities and their vulnerability to global changes threats. Here we introduce University, USA a photosymbiotic tidal acoel flatworm, Symsagittifera roscoffensis, and its obligatory *Correspondence: green algal photosymbiont, Tetraselmis convolutae (Lack of the algal partner invariably Xavier Bailly, Station Biologique de results in acoel lethality emphasizing the mandatory nature of the photosymbiotic Roscoff, Place Georges Teissier, 29680 Roscoff, France algae for the animal’s survival). Together they form a composite photosymbiotic unit, e-mail: [email protected] which can be reared in controlled conditions that provide easy access to key life-cycle events ranging from early embryogenesis through the induction of photosymbiosis in aposymbiotic juveniles to the emergence of a functional “solar-powered” mature stage. Since it is possible to grow both algae and host under precisely controlled culture conditions, it is now possible to design a range of new experimental protocols that address the mechanisms and evolution of photosymbiosis. S. roscoffensis thus represents an emerging model system with experimental advantages that complement those of other photosymbiotic species, in particular corals. The basal taxonomic position of S. roscoffensis (and acoels in general) also makes it a relevant model for evolutionary studies of development, stem cell biology and regeneration. Finally, it’s autotrophic lifestyle and lack of calcification make S. roscoffensis a favorable system to study the role of symbiosis in the response of marine organisms to climate change (e.g., ocean warming and acidification). In this article we summarize the state of knowledge of the biology of S. roscoffensis and its algal partner from studies dating back over a century, and provide an overview of ongoing research efforts that take advantage of this unique system. Keywords: acoel, roscoffensis, symbiosis, regeneration, brain, algae, tetraselmis, model INTRODUCTION photosymbiotic protists (unicellular eukaryotes) from the tax- Photosymbiosis represents around 50% of marine photosyn- onomic super-groups Rhizaria, Alveolates, and Stramenopiles thesis, as exemplified by corals and other reef animals as (Baldauf, 2008). An association between a host (multi- or uni- well as by the remarkable biomass and diversity of oceanic cellular) and an “algal” photosymbiont represents, in principle, www.frontiersin.org October 2014 | Volume 5 | Article 498 | 1 Bailly et al. An emerging photosymbiotic model a “domestication” of photosynthesis that can result in a trophic including development, ecology, and genetics. This lack of exper- independence as long as the partners are located in the euphotic imental progress is especially unfortunate for issues in metazoan zone in view of the infinite source of solar energy. As a con- evolution. This is because S. roscoffensis as an acoel represents sequence, photosymbiosis has a strong global ecological impact something of a Gordian knot in the debate concerning the and, hence, the adaptations and innovations that contribute to features of the ancestor of the all bilaterian animals (the so- photosymbiotic interactions require both in depth functional called “urbilaterian”). In this debate some scientists propose that and molecular analysis. This analysis is also important since all Bilateria are descendants of a primitively coelomate ances- the evolutionary success of photosymbiosis, based on inno- tor (archicoelomate hypothesis, Salvini-Plawen, 1978; Balavoine, vative combinations of hosts/photosynthetic symbionts, con- 1998) implying that flatworms have secondarily lost their coelom tributes markedly to marine diversity. Finally, a comprehensive and are thus not basal bilaterians, while others argue that acoel understanding of the mechanisms underlying the recruitment of flatworms are primarily simple and that their acoelomate condi- photosynthetic symbionts by heterotrophic organisms may also tion is representative of the ancestor of the Bilateria (planuloid- contribute to and understanding of the ancestral evolutionary acoeloid hypothesis, Salvini-Plawen, 1978; Baguna and Riutort, events of acquisition of plastid-like endosymbionts by a prim- 2004a). itive heterotrophic eukaryotic cells, i.e., primary and secondary Thus, from a historical point of view, the current renaissance in endosymbiosis. experimental investigations of S. roscoffensis represents a renewal We introduce here Symsagittifera roscoffensis (formerly with a rich and relevant background of over a century of studies Convoluta roscoffensis), a marine flatworm-like animal that dedicated to this acoel flatworm from the early 1870s until the belongs to the phylum Acoela (a = non, coela = cavity), as 1980s. In this report, we review the current state of knowledge an ideal photosymbiotic biological model system for exploring concerning the biology, ecology, and physiology of this animal, the functional biology, molecular biology and evolution of and we highlight the many new avenues of research made possible photosymbioses. S. roscoffensis, described as a “Plant-Animal” by the precise experimental control of the ontogeny of this marine (Keebles, 1910) a century ago, is endemic to the intertidal zone of flatworm including induced symbiogenesis through co-culture of European coasts of the Atlantic Ocean and the English Channel, the acoel and the algal symbiont. and at low tide forms huge colonies composed of millions of individuals (Figures 1, 2A–C). The vivid green color of the HISTORICAL BACKGROUND ON S. ROSCOFFENSIS AND ITS colonies is due to the abundant presence of a unicellular green SYMBIONT algal endosymbiont, namely the prasinophyte Tetraselmis con- Studies beginning in the late nineteenth century centered on volutae (Figure 3A). This animal presents a wealth of biological the origin and the role of the enigmatic “green cells” inhabiting
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