The enigmatic association of photosynthetically active chloroplasts from algae and some sacoglossan sea slugs, called functional kleptoplasty, is a functional unique system of photosymbioses observed in metazoans. Besides the specific adaptations of the slugs necessary to incorporate and maintain the plastids, the organelles need to ensure optimal photosynthesis. Photoprotective mechanisms in the plastids, namely the xanthophyll cycle (XC) and the high-energy dependent quenching (q E ) part of the non-photochemical quenching (NPQ), and the repair of the D1 protein of Photosystem II (PSII) are considered crucial for kleptoplast longevity in the slugs. Here, we studied the sea slugs Elysia viridis fed with the naturally occurring XC and q E -deficient Bryopsis hypnoides, and E. timida fed on Acetabularia acetabulum, an alga that possesses both mechanisms. The aim of the study was to understand (i) whether q E remains active after ingestion of kleptoplasts by E. timida, (ii) how different light intensities affect the photosynthetic activity of kleptoplasts with and without photoprotection mechanisms, and (iii) if the kleptoplasts are able to repair photodamaged D1 protein. With regard to NPQ, freshly incorporated kleptoplasts responded to different light stress in the same manner as the chloroplasts in their native host algae. Even after 3 weeks of incorporation the q E part of NPQ was present in the kleptoplasts of E. timida. However, the presence of the q E component of NPQ did not prevent the kleptoplasts from significant PSII photoinactivation under high light intensities. This is probably due to the fact that the kleptoplasts have a reduced PSII repair capacity, despite plastid encoded repair mechanisms in every sacoglossan food source. Hence, photoprotective mechanisms are probably not a key factor explaining kleptoplast longevity in Sacoglossa sea slugs.
Summary: UniMoG is a software combining five genome rearrangement models: double cut and join (DCJ), restricted DCJ, Hannenhalli and Pevzner (HP), inversion and translocation. It can compute the pairwise genomic distances and a corresponding optimal sorting scenario for an arbitrary number of genomes. All five models can be unified through the DCJ model, thus the implementation is based on DCJ and, where reasonable, uses the most efficient existing algorithms for each distance and sorting problem. Both textual and graphical output is possible for visualizing the operations.Availability and implementation: The software is available through the Bielefeld University Bioinformatics Web Server at http://bibiserv.techfak.uni-bielefeld.de/dcj with instructions and example data.Contact: rhilker@cebitec.uni-bielefeld.de
Symbiosis with photoautotrophic organisms has evolved in various species and even whole animal lineages, which allowed them to directly benefit from photosynthesis. This so-called photosymbiosis is best studied in cnidarians, which primarily establish symbioses with dinoflagellates from the family Symbiodiniaceae. In most other animals the mechanisms of establishing photosymbiosis, the physiological basis, and the evolution of a photosymbiotic life history remain poorly understood. Sea slugs belonging to the Cladobranchia (Gastropoda, Nudibranchia) are no exception, and are a rather neglected animal lineage in the research field of photosymbiosis. Yet, studying these sea slugs holds great potential to establish a unique photosymbiosis model, as they are the only known taxon that has evolved two different strategies to acquire their symbiont: either from cnidarian prey (thus becoming a secondary host) or directly out of the water column. The mechanisms for photobiont uptake and maintenance are unknown for these sea slugs, but might be similar to those of cnidarians. However, in terms of the evolution of photosymbiosis, Cladobranchia seem to share many commonalities with more closely related sea slugs belonging to the Sacoglossa, which only maintain the chloroplasts of the algae they feed on. Hence, Cladobranchia have the potential to shed light on the evolution of photosymbiosis in taxonomically divergent animals that also harbor photobionts of different evolutionary lineages.
Photosymbiosis is found in different animal lineages and is best understood in cnidarians. A successful initiation and maintenance of the symbiosis between the animal hosts and the photosymbiotic partners is based on a recognition by specific host receptors. This triggers signaling cascades that promote the photobiont tolerance by the host, including an interpartner nutrient exchange and the ability of the host to cope with increased levels of reactive oxygen species (ROS) generated by the photobiont. Key to the successful symbiosis is the inhibition of the phagosomal maturation resulting in the formation of the symbiosome. In animals other than cnidarians, little is known about the photosymbiosis initiation and maintenance, for instance in sea slugs belonging to the Nudibranchia. Here, we investigated the gene expression profile of Berghia stephanieae, which is able to incorporate Breviolum minutum from its cnidarian prey Exaiptasia diaphana (Rapp, 1829) but is not able to maintain the algae for more than a couple of days during starvation. We show that the recognition of the algae is based on similar mechanisms present in cnidarians, and we identified some additional candidate genes that might be molluscan specific for photobiont recognition. Downstream, B. stephanieae responds to increased levels of ROS but is not able to stop the phagosomal maturation or decrease the immune response against B. minutum, which seem to be the key factors missing in B. stephanieae that accounts for the unstable symbiosis in this slug. Hence, B. stephanieae can be considered a transitional state toward a stable photosymbiosis and can help to elucidate general aspects of the evolutionary processes involved in establishing photosymbioses in animals.
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