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      Synthetic symbiosis between a cyanobacterium and a ciliate toward novel chloroplast-like endosymbiosis

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          Abstract

          Chloroplasts are thought to have co-evolved through endosymbiosis, after a cyanobacterial-like prokaryote was engulfed by a eukaryotic cell; however, it is impossible to observe the process toward chloroplasts. In this study, we constructed an experimental symbiosis model to observe the initial stage in the process from independent organisms to a chloroplast-like organelle. Our system of synthetic symbiosis is capable of long-term coculture of two model organisms: a cyanobacterium ( Synechocystis sp. PCC6803) as a symbiont and a ciliate ( Tetrahymena thermophila) as a host with endocytic ability. The experimental system was clearly defined, because we used a synthetic medium and the cultures were shaken to avoid spatial complexity. We determined the experimental conditions for sustainable coculture, by analyzing population dynamics using a mathematical model. We experimentally demonstrated that the coculture was sustainable for at least 100 generations, through serial transfers. Moreover, we found that cells isolated after the serial transfer improved the probability of coexistence of both species without extinction in re-coculture. The constructed system will be useful for understanding the initial stage of primary endosymbiosis from cyanobacteria to chloroplasts, i.e., the origin of algae and plants.

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          Purification and properties of unicellular blue-green algae (order Chroococcales).

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            On the origin of mitosing cells

            Lynn Sagan (1967)
            A theory of the origin of eukaryotic cells ("higher" cells which divide by classical mitosis) is presented. By hypothesis, three fundamental organelles: the mitochondria, the photosynthetic plastids and the (9+2) basal bodies of flagella were themselves once free-living (prokaryotic) cells. The evolution of photosynthesis under the anaerobic conditions of the early atmosphere to form anaerobic bacteria, photosynthetic bacteria and eventually blue-green algae (and protoplastids) is described. The subsequent evolution of aerobic metabolism in prokaryotes to form aerobic bacteria (protoflagella and protomitochondria) presumably occurred during the transition to the oxidizing atmosphere. Classical mitosis evolved in protozoan-type cells millions of years after the evolution of photosynthesis. A plausible scheme for the origin of classical mitosis in primitive amoeboflagellates is presented. During the course of the evolution of mitosis, photosynthetic plastids (themselves derived from prokaryotes) were symbiotically acquired by some of these protozoans to form the eukaryotic algae and the green plants. The cytological, biochemical and paleontological evidence for this theory is presented, along with suggestions for further possible experimental verification. The implications of this scheme for the systematics of the lower organisms is discussed.
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              DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis.

              In eukaryotes, DNA is exchanged between endosymbiosis-derived compartments (mitochondria and chloroplasts) and the nucleus. Organelle-to-nucleus DNA transfer involves repair of double-stranded breaks by nonhomologous end-joining, and resulted during early organelle evolution in massive relocation of organelle genes to the nucleus. A large fraction of the products of the nuclear genes so acquired are retargeted to their ancestral compartment; many others now function in new subcellular locations. Almost all present-day nuclear transfers of mitochondrial or plastid DNA give rise to noncoding sequences, dubbed nuclear mitochondrial DNAs (NUMTs) and nuclear plastid DNAs (NUPTs). Some of these sequences were recruited as exons, thus introducing new coding sequences into preexisting nuclear genes by a novel mechanism. In organisms derived from secondary or tertiary endosymbiosis, serial gene transfers involving nucleus-to-nucleus migration of DNA have also occurred. Intercompartmental DNA transfer therefore represents a significant driving force for gene and genome evolution, relocating and refashioning genes and contributing to genetic diversity.
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                Author and article information

                Contributors
                azumay@iph.osaka.jp
                hosodak@nict.go.jp
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                13 April 2023
                13 April 2023
                2023
                : 13
                : 6104
                Affiliations
                [1 ]GRID grid.136593.b, ISNI 0000 0004 0373 3971, Institute for Transdisciplinary Graduate Degree Programs, , Osaka University, ; 1-5 Yamadaoka, Suita, Osaka 565-0871 Japan
                [2 ]GRID grid.136593.b, ISNI 0000 0004 0373 3971, Graduate School of Information Science and Technology, , Osaka University, ; 1-5 Yamadaoka, Suita, Osaka 565-0871 Japan
                [3 ]GRID grid.416993.0, ISNI 0000 0004 0629 2067, Division of Hygienic Chemistry, , Osaka Institute of Public Health, ; 1-3-3 Nakamichi, Higashinari-ku, Osaka, 537-0025 Japan
                [4 ]GRID grid.26999.3d, ISNI 0000 0001 2151 536X, Universal Biology Institute, Graduate School of Science, , The University of Tokyo, ; 7-3-1 Hongo, Bunkyo-Ku, Tokyo, 113-0033 Japan
                [5 ]GRID grid.136593.b, ISNI 0000 0004 0373 3971, Graduate School of Frontier Biosciences, , Osaka University, ; Suita, Osaka 565-0871 Japan
                [6 ]GRID grid.508743.d, RIKEN Center for Biosystems Dynamics Research, ; 6-2-3 Furuedai, Suita, Osaka 565-0874 Japan
                [7 ]GRID grid.28312.3a, ISNI 0000 0001 0590 0962, Center for Information and Neural Networks (CiNet), , National Institute of Information and Communications Technology (NICT), ; Osaka, Japan
                Article
                33321
                10.1038/s41598-023-33321-w
                10102011
                37055487
                913a9128-ecd9-4a7c-8fb5-72adb8d31d6a
                © The Author(s) 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
                : 9 February 2023
                : 11 April 2023
                Funding
                Funded by: JSPS KAKENHI
                Award ID: JP18H04821
                Award Recipient :
                Categories
                Article
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                © The Author(s) 2023

                Uncategorized
                ecology,evolution,systems biology
                Uncategorized
                ecology, evolution, systems biology

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