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      Negative phototaxis in the photosymbiotic sea anemone Aiptasia as a potential strategy to protect symbionts from photodamage

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          Abstract

          Photosymbiotic cnidarians generally seek bright environments so that their symbionts can be photosynthetically active. However, excess light may result in a breakdown of symbiosis due to the accumulation of photodamage in symbionts causing symbiont loss (bleaching). It is currently unknown if photosymbiotic cnidarians sense light only to regulate spawning time and to facilitate predation, or whether they also use their light-sensing capacities to protect their symbionts from photodamage. In this study, we examined how the sea anemone Aiptasia changes its behaviour when exposed to excess light. We reveal that Aiptasia polyps, when carrying symbionts, contract their bodies when exposed to high light intensities and subsequently migrate away in a direction perpendicular to the light source. Interestingly, this negative phototaxis was only evident under blue light and absent upon UV, green and red light exposure. Non-symbiotic Aiptasia did not exhibit this light response. Our study demonstrates that photosymbiotic Aiptasia polyps display negative phototactic behaviour in response to blue light, and that they also can perceive its direction, despite lacking specialized eye structures. We postulate that Aiptasia uses blue light, which penetrates seawater efficiently, as a general proxy for sunlight exposure to protect its symbionts from photodamage.

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          Most cited references20

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          Cell biology of cnidarian-dinoflagellate symbiosis.

          The symbiosis between cnidarians (e.g., corals or sea anemones) and intracellular dinoflagellate algae of the genus Symbiodinium is of immense ecological importance. In particular, this symbiosis promotes the growth and survival of reef corals in nutrient-poor tropical waters; indeed, coral reefs could not exist without this symbiosis. However, our fundamental understanding of the cnidarian-dinoflagellate symbiosis and of its links to coral calcification remains poor. Here we review what we currently know about the cell biology of cnidarian-dinoflagellate symbiosis. In doing so, we aim to refocus attention on fundamental cellular aspects that have been somewhat neglected since the early to mid-1980s, when a more ecological approach began to dominate. We review the four major processes that we believe underlie the various phases of establishment and persistence in the cnidarian/coral-dinoflagellate symbiosis: (i) recognition and phagocytosis, (ii) regulation of host-symbiont biomass, (iii) metabolic exchange and nutrient trafficking, and (iv) calcification. Where appropriate, we draw upon examples from a range of cnidarian-alga symbioses, including the symbiosis between green Hydra and its intracellular chlorophyte symbiont, which has considerable potential to inform our understanding of the cnidarian-dinoflagellate symbiosis. Ultimately, we provide a comprehensive overview of the history of the field, its current status, and where it should be going in the future.
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            Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis.

            Cnidarian bleaching is a breakdown in the mutualistic symbiosis between host Cnidarians, such as reef building corals, and their unicellular photosynthetic dinoflagellate symbionts. Bleaching is caused by a variety of environmental stressors, most notably elevated temperatures associated with global climate change in conjunction with high solar radiation, and it is a major contributor to coral death and reef degradation. This review examines the underlying cellular events that lead to symbiosis dysfunction and cause bleaching, emphasizing that, to date, we have only some pieces of a complex cellular jigsaw puzzle. Reactive oxygen species (ROS), generated by damage to both photosynthetic and mitochondrial membranes, is shown to play a central role in both injury to the partners and to inter-partner communication of a stress response. Evidence is presented that suggests that bleaching is a host innate immune response to a compromised symbiont, much like innate immune responses in other host-microbe interactions. Finally, the elimination or exit of the symbiont from host tissues is described through a variety of mechanisms including exocytosis, host cell detachment and host cell apoptosis.
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              Oxidative stress causes coral bleaching during exposure to elevated temperatures

              M. Lesser (1997)
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                Author and article information

                Contributors
                nicholas.foulkes@kit.edu
                annika.guse@biologie.uni-muenchen.de
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                19 October 2023
                19 October 2023
                2023
                : 13
                : 17857
                Affiliations
                [1 ]National Institute for Basic Biology, ( https://ror.org/05q8wtt20) Nishigonaka 38, Myodaiji, Okazaki, Aichi 444-8585 Japan
                [2 ]Centre for Organismal Studies, Heidelberg University, ( https://ror.org/038t36y30) Im Neuenheimer Feld 230, 69120 Heidelberg, Germany
                [3 ]Present Address: Department of Translational Genomics, Medical Faculty, University of Cologne, ( https://ror.org/00rcxh774) Weyertal 115b, 50931 Cologne, Germany
                [4 ]Institute of Biological and Chemical Systems, Karlsruhe Institute of Technology, ( https://ror.org/04t3en479) 76344 Eggenstein-Leopoldshafen, Germany
                [5 ]Present Address: Faculty of Biology, Ludwig-Maximilians-Universität München, ( https://ror.org/05591te55) Großhadernerstr. 2, 82152 Planegg-Martinsried, Germany
                Article
                44583
                10.1038/s41598-023-44583-9
                10587101
                37857737
                17fd0aec-ec78-43e8-b615-ce83e56b9f97
                © Springer Nature Limited 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 11 August 2023
                : 10 October 2023
                Funding
                Funded by: Government of Canada
                Award ID: NFRFE-2019-00189
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: 724715
                Award Recipient :
                Funded by: Ludwig-Maximilians-Universität München (1024)
                Categories
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                © Springer Nature Limited 2023

                Uncategorized
                ecology,behavioural ecology,ecophysiology,microbial communities,symbiosis
                Uncategorized
                ecology, behavioural ecology, ecophysiology, microbial communities, symbiosis

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