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      Evolution of heterotrophy in chrysophytes as reflected by comparative transcriptomics

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          ABSTRACT

          Shifts in the nutritional mode between phototrophy, mixotrophy and heterotrophy are a widespread phenomenon in the evolution of eukaryotic diversity. The transition between nutritional modes is particularly pronounced in chrysophytes and occurred independently several times through parallel evolution. Thus, chrysophytes provide a unique opportunity for studying the molecular basis of nutritional diversification and of the accompanying pathway reduction and degradation of plastid structures. In order to analyze the succession in switching the nutritional mode from mixotrophy to heterotrophy, we compared the transcriptome of the mixotrophic Poterioochromonas malhamensis with the transcriptomes of three obligate heterotrophic species of Ochromonadales. We used the transcriptome of P. malhamensis as a reference for plastid reduction in the heterotrophic taxa. The analyzed heterotrophic taxa were in different stages of plastid reduction. We investigated the reduction of several photosynthesis related pathways e.g. the xanthophyll cycle, the mevalonate pathway, the shikimate pathway and the tryptophan biosynthesis as well as the reduction of plastid structures and postulate a presumable succession of pathway reduction and degradation of accompanying structures.

          Abstract

          Different pathway repertoirs in heterotrophic chrysophytes indicate the stepwise loss of photosynthesis related pathways in the course of evolution of heterotrophy.

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          Most cited references63

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          THE SHIKIMATE PATHWAY.

          The shikimate pathway links metabolism of carbohydrates to biosynthesis of aromatic compounds. In a sequence of seven metabolic steps, phosphoenolpyruvate and erythrose 4-phosphate are converted to chorismate, the precursor of the aromatic amino acids and many aromatic secondary metabolites. All pathway intermediates can also be considered branch point compounds that may serve as substrates for other metabolic pathways. The shikimate pathway is found only in microorganisms and plants, never in animals. All enzymes of this pathway have been obtained in pure form from prokaryotic and eukaryotic sources and their respective DNAs have been characterized from several organisms. The cDNAs of higher plants encode proteins with amino terminal signal sequences for plastid import, suggesting that plastids are the exclusive locale for chorismate biosynthesis. In microorganisms, the shikimate pathway is regulated by feedback inhibition and by repression of the first enzyme. In higher plants, no physiological feedback inhibitor has been identified, suggesting that pathway regulation may occur exclusively at the genetic level. This difference between microorganisms and plants is reflected in the unusually large variation in the primary structures of the respective first enzymes. Several of the pathway enzymes occur in isoenzymic forms whose expression varies with changing environmental conditions and, within the plant, from organ to organ. The penultimate enzyme of the pathway is the sole target for the herbicide glyphosate. Glyphosate-tolerant transgenic plants are at the core of novel weed control systems for several crop plants.
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            The endosymbiotic origin, diversification and fate of plastids.

            Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.
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              Plastid evolution.

              The ancestors of modern cyanobacteria invented O(2)-generating photosynthesis some 3.6 billion years ago. The conversion of water and CO(2) into energy-rich sugars and O(2) slowly transformed the planet, eventually creating the biosphere as we know it today. Eukaryotes didn't invent photosynthesis; they co-opted it from prokaryotes by engulfing and stably integrating a photoautotrophic prokaryote in a process known as primary endosymbiosis. After approximately a billion of years of coevolution, the eukaryotic host and its endosymbiont have achieved an extraordinary level of integration and have spawned a bewildering array of primary producers that now underpin life on land and in the water. No partnership has been more important to life on earth. Secondary endosymbioses have created additional autotrophic eukaryotic lineages that include key organisms in the marine environment. Some of these organisms have subsequently reverted to heterotrophic lifestyles, becoming significant pathogens, microscopic predators, and consumers. We review the origins, integration, and functions of the different plastid types with special emphasis on their biochemical abilities, transfer of genes to the host, and the back supply of proteins to the endosymbiont.
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                Author and article information

                Journal
                FEMS Microbiol Ecol
                FEMS Microbiol. Ecol
                femsec
                FEMS Microbiology Ecology
                Oxford University Press
                0168-6496
                1574-6941
                06 March 2018
                April 2018
                06 March 2018
                : 94
                : 4
                : fiy039
                Affiliations
                [1 ]Biodiversity, Faculty of Biology, University of Duisburg-Essen, Universitätsstr. 5, D-45141 Essen, Germany
                [2 ]Genome Informatics, Institute of Human Genetics, University of Duisburg-Essen, University Hospital Essen, Hufelandstr. 55, D-45147 Essen, Germany
                [3 ]Centre for Water and Environmental Research (ZWU), University of Duisburg-Essen, Universitätsstr. 2, D-45141 Essen, Germany
                Author notes
                Corresponding author: Nadine Graupner, Biodiversity, University of Duisburg-Essen, Universitätsstr. 5, D-45141 Essen, Germany. Tel: +49-201-183-3442; Fax: +49-201-183-4290; E-mail: nadine.graupner@ 123456uni-due.de
                Author information
                http://orcid.org/0000-0002-8536-6065
                Article
                fiy039
                10.1093/femsec/fiy039
                6019013
                29518196
                a5bee350-650e-4f10-a135-6581bdf09227
                © FEMS 2018.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 05 March 2018
                : 27 November 2017
                Page count
                Pages: 11
                Funding
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Award ID: BO 3245/17
                Award ID: BO 3245/14
                Funded by: Mercator Research Center Ruhr
                Award ID: Pe-2013-0012
                Categories
                Research Article

                Microbiology & Virology
                spumella vulgaris,poteriospumella lacustris,pedospumella encystans,heterotrophic nanoflagellates (hnf),chrysomonad flagellates,evolutionary ecology,plastid reduction,non-photosynthetic plastids,transcriptome

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