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      Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

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          Abstract

          Coral–dinoflagellate symbiosis underpins the evolutionary success of corals reefs. Successful exchange of molecules between the cnidarian host and the Symbiodiniaceae algae enables the mutualistic partnership. The algae translocate photosynthate to their host in exchange for nutrients and shelter. The photosynthate must traverse multiple membranes, most likely facilitated by transporters. Here, we compared gene expression profiles of cultured, free‐living Breviolum minutum with those of the homologous symbionts freshly isolated from the sea anemone Exaiptasia diaphana, a widely used model for coral hosts. Additionally, we assessed expression levels of a list of candidate host transporters of interest in anemones with and without symbionts. Our transcriptome analyses highlight the distinctive nature of the two algal life stages, with many gene expression level changes correlating to the different morphologies, cell cycles, and metabolisms adopted in hospite versus free‐living. Morphogenesis‐related genes that likely underpin the metamorphosis process observed when symbionts enter a host cell were up‐regulated. Conversely, many down‐regulated genes appear to be indicative of the protective and confined nature of the symbiosome. Our results emphasize the significance of transmembrane transport to the symbiosis, and in particular of ammonium and sugar transport. Further, we pinpoint and characterize candidate transporters—predicted to be localized variously to the algal plasma membrane, the host plasma membrane, and the symbiosome membrane—that likely serve pivotal roles in the interchange of material during symbiosis. Our study provides new insights that expand our understanding of the molecular exchanges that underpin the cnidarian–algal symbiotic relationship.

          Abstract

          The symbiosis between corals and dinoflagellate algae underpins the evolutionary success of corals reefs. Our study focuses on algal symbiont gene expression and targets differentially expressed putative transporters that might serve pivotal roles in the interchange of material during symbiosis. Our study emphasizes the great significance of transmembrane transport to the success of the symbiotic relationship.

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          Most cited references96

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          Sugar transporters for intercellular exchange and nutrition of pathogens.

          Sugar efflux transporters are essential for the maintenance of animal blood glucose levels, plant nectar production, and plant seed and pollen development. Despite broad biological importance, the identity of sugar efflux transporters has remained elusive. Using optical glucose sensors, we identified a new class of sugar transporters, named SWEETs, and show that at least six out of seventeen Arabidopsis, two out of over twenty rice and two out of seven homologues in Caenorhabditis elegans, and the single copy human protein, mediate glucose transport. Arabidopsis SWEET8 is essential for pollen viability, and the rice homologues SWEET11 and SWEET14 are specifically exploited by bacterial pathogens for virulence by means of direct binding of a bacterial effector to the SWEET promoter. Bacterial symbionts and fungal and bacterial pathogens induce the expression of different SWEET genes, indicating that the sugar efflux function of SWEET transporters is probably targeted by pathogens and symbionts for nutritional gain. The metazoan homologues may be involved in sugar efflux from intestinal, liver, epididymis and mammary cells.
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            Systematic and Biogeographical Patterns in the Reproductive Biology of Scleractinian Corals

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              The genome of Aiptasia, a sea anemone model for coral symbiosis.

              The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between a cnidarian animal host (the coral) and intracellular photosynthetic dinoflagellate algae. The molecular and cellular mechanisms underlying this endosymbiosis are not well understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable laboratory model for investigating these mechanisms. Here we report on the assembly and analysis of the Aiptasia genome, which will provide a foundation for future studies and has revealed several features that may be key to understanding the evolution and function of the endosymbiosis. These features include genomic rearrangements and taxonomically restricted genes that may be functionally related to the symbiosis, aspects of host dependence on alga-derived nutrients, a novel and expanded cnidarian-specific family of putative pattern-recognition receptors that might be involved in the animal-algal interactions, and extensive lineage-specific horizontal gene transfer. Extensive integration of genes of prokaryotic origin, including genes for antimicrobial peptides, presumably reflects an intimate association of the animal-algal pair also with its prokaryotic microbiome.
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                Author and article information

                Contributors
                Keren.Maor@live.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                12 December 2019
                January 2020
                : 10
                : 1 ( doiID: 10.1002/ece3.v10.1 )
                : 451-466
                Affiliations
                [ 1 ] School of BioSciences The University of Melbourne Melbourne Vic. Australia
                [ 2 ] Australian Institute of Marine Science Townsville Qld Australia
                Author notes
                [*] [* ] Correspondence

                Keren Maor‐Landaw, School of BioSciences, The University of Melbourne, Parkville, Melbourne, Vic. 3010, Australia.

                Email: Keren.Maor@ 123456live.com

                Author information
                https://orcid.org/0000-0002-0485-6119
                Article
                ECE35910
                10.1002/ece3.5910
                6972872
                31993121
                bf33d454-ba70-4bcf-ae02-9a059a6efc5e
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 10 October 2019
                : 25 October 2019
                : 18 November 2019
                Page count
                Figures: 4, Tables: 0, Pages: 16, Words: 12961
                Funding
                Funded by: Australian Research Council Discovery Project
                Award ID: DP160101539
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                January 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.5 mode:remove_FC converted:21.01.2020

                Evolutionary Biology
                breviolum minutum,exaiptasia diaphana,free‐living,in hospite,symbiosis,transporters

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