The chimerical and multifaceted marine acoel Symsagittifera roscoffensis: from photosymbiosis to brain regeneration

Abstract

A remarkable example of biological engineering is the capability of some marine animals to take advantage of photosynthesis by hosting symbiotic algae. This capacity, referred to as photosymbiosis, is based on structural and functional complexes that involve two distantly unrelated organisms. These stable photosymbiotic associations between metazoans and photosynthetic protists play fundamental roles in marine ecology as exemplified by reef communities and their vulnerability to global changes threats. Here we introduce a photosymbiotic tidal acoel flatworm, Symsagittifera roscoffensis, and its obligatory green algal photosymbiont, Tetraselmis convolutae (Lack of the algal partner invariably results in acoel lethality emphasizing the mandatory nature of the photosymbiotic algae for the animal's survival). Together they form a composite photosymbiotic unit, 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.

Social behaviour and collective motion in plant-animal worms

“…We hypothesize these mats enable the worms to stabilize their positions in pools of seepage sea water on sandy beaches (figure 4b), by sharing a more or less continuous mucous sheath. The sharing of such a relatively thick mucous sheet may also enable the worms to benefit from sunlight on both of their sides at once as their underside receives solar energy reflected from the substrate [8].…”

“…B 283: 20152946 aggregations as living shields against environmental extremes, is seen, for example, in emperor penguins who form rotating huddles as protection against extreme Antarctic winds [30,31]. The worms are likely to find greater individual safety in these hugely dense aggregations and may even be able to defend themselves collectively through the mass production of dimethylsulfoniopropionate [8,32,33].…”

“…Hence, they seek sites where their algae can photosynthesize [9] more effectively. These worms are typically encountered as biofilms on sandy beaches at low tide [8]. In initial observations of S. roscoffensis transferred at fairly high densities to Petri dishes containing a shallow pool of sea water, we noted a rapid and spontaneous emergence of circular milling behaviour, which, to the best of our knowledge, had not been described before in these worms, very possibly because it may occur only fleetingly at a certain stage of the tidal cycle, for example when S. roscoffensis initially come to the surface on the beaches they inhabit.…”

Genealogical correspondence of a forebrain centre implies an executive brain in the protostome–deuterostome bilaterian ancestor

“…To answer this question we selected amongst Xenacoelomorpha the acoel S. roscoffensis, which, recent studies demonstrate, possesses a ganglionic area rostrally from which extend caudally directed nerve cords and nerve nets that are resolved using antisera against neural proteins and peptides [78][79][80]. Application of antisera against the Drosophila PKA-Ca orthologue, DC0, as well as phosphorylated Ca 2þ /calmodulin-dependent protein kinase II ( pCaMKII) to S. roscoffensis shows a substantial and bilaterally symmetric domain expressing high levels of these proteins at this anterior neuronal domain and low levels of the proteins distributed through other tissues, as would be expected.…”

“…Abundant chemosensory receptors on the acoel's epidermis would be disposed to provide numerous axons to the DC0-positive domain, possible via extensive processes revealed by antisera against elav and synaptotagmin that converge there [67]. The DC0 and pCaMKII domains coincide in part with a second bilateral system expressing serotonin that also extends axon bundles caudally [78,79]. However, the DC0/pCaMKII domain is constrained anteriorly and does not extend into rostrally directed nerve cords.…”