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      Carbon/nitrogen homeostasis control in cyanobacteria

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          ABSTRACT

          Carbon/nitrogen (C/N) balance sensing is a key requirement for the maintenance of cellular homeostasis. Therefore, cyanobacteria have evolved a sophisticated signal transduction network targeting the metabolite 2-oxoglutarate (2-OG), the carbon skeleton for nitrogen assimilation. It serves as a status reporter for the cellular C/N balance that is sensed by transcription factors NtcA and NdhR and the versatile PII-signaling protein. The PII protein acts as a multitasking signal-integrating regulator, combining the 2-OG signal with the energy state of the cell through adenyl-nucleotide binding. Depending on these integrated signals, PII orchestrates metabolic activities in response to environmental changes through binding to various targets. In addition to 2-OG, other status reporter metabolites have recently been discovered, mainly indicating the carbon status of the cells. One of them is cAMP, which is sensed by the PII-like protein SbtB. The present review focuses, with a main emphasis on unicellular model strains Synechoccus elongatus and Synechocystis sp. PCC 6803, on the physiological framework of these complex regulatory loops, the tight linkage to metabolism and the molecular mechanisms governing the signaling processes.

          Abstract

          This review presents the current knowledge on the sophisticated signal transduction network evolved in cyanobacteria to maintain carbon/nitrogen homeostasis.

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          Most cited references201

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          Evolution of photosynthesis.

          Energy conversion of sunlight by photosynthetic organisms has changed Earth and life on it. Photosynthesis arose early in Earth's history, and the earliest forms of photosynthetic life were almost certainly anoxygenic (non-oxygen evolving). The invention of oxygenic photosynthesis and the subsequent rise of atmospheric oxygen approximately 2.4 billion years ago revolutionized the energetic and enzymatic fundamentals of life. The repercussions of this revolution are manifested in novel biosynthetic pathways of photosynthetic cofactors and the modification of electron carriers, pigments, and existing and alternative modes of photosynthetic carbon fixation. The evolutionary history of photosynthetic organisms is further complicated by lateral gene transfer that involved photosynthetic components as well as by endosymbiotic events. An expanding wealth of genetic information, together with biochemical, biophysical, and physiological data, reveals a mosaic of photosynthetic features. In combination, these data provide an increasingly robust framework to formulate and evaluate hypotheses concerning the origin and evolution of photosynthesis.
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            Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor.

            Spermatozoa undergo a poorly understood activation process induced by bicarbonate and mediated by cyclic adenosine 3',5'-monophosphate (cAMP). It has been assumed that bicarbonate mediates its effects through changes in intracellular pH or membrane potential; however, we demonstrate here that bicarbonate directly stimulates mammalian soluble adenylyl cyclase (sAC) activity in vivo and in vitro in a pH-independent manner. sAC is most similar to adenylyl cyclases from cyanobacteria, and bicarbonate regulation of cyclase activity is conserved in these early forms of life. sAC is also expressed in other bicarbonate-responsive tissues, which suggests that bicarbonate regulation of cAMP signaling plays a fundamental role in many biological systems.
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              Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants.

              Cyanobacteria have evolved a significant environmental adaptation, known as a CO(2)-concentrating-mechanism (CCM), that vastly improves photosynthetic performance and survival under limiting CO(2) concentrations. The CCM functions to transport and accumulate inorganic carbon actively (Ci; HCO(3)(-), and CO(2)) within the cell where the Ci pool is utilized to provide elevated CO(2) concentrations around the primary CO(2)-fixing enzyme, ribulose bisphosphate carboxylase-oxygenase (Rubisco). In cyanobacteria, Rubisco is encapsulated in unique micro-compartments known as carboxysomes. Cyanobacteria can possess up to five distinct transport systems for Ci uptake. Through database analysis of some 33 complete genomic DNA sequences for cyanobacteria it is evident that considerable diversity exists in the composition of transporters employed, although in many species this diversity is yet to be confirmed by comparative phenomics. In addition, two types of carboxysomes are known within the cyanobacteria that have apparently arisen by parallel evolution, and considerable progress has been made towards understanding the proteins responsible for carboxysome assembly and function. Progress has also been made towards identifying the primary signal for the induction of the subset of CCM genes known as CO(2)-responsive genes, and transcriptional regulators CcmR and CmpR have been shown to regulate these genes. Finally, some prospects for introducing cyanobacterial CCM components into higher plants are considered, with the objective of engineering plants that make more efficient use of water and nitrogen.
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                Author and article information

                Contributors
                Journal
                FEMS Microbiol Rev
                FEMS Microbiol Rev
                femsre
                FEMS Microbiology Reviews
                Oxford University Press
                0168-6445
                1574-6976
                January 2020
                16 October 2019
                16 October 2019
                : 44
                : 1
                : 33-53
                Affiliations
                Lehrstuhl für Mikrobiologie , Universität Tübingen, Auf der Morgenstelle 28, D-72076 Tübingen, Germany
                Lehrstuhl für Mikrobiologie , Universität Tübingen, Auf der Morgenstelle 28, D-72076 Tübingen, Germany
                Author notes
                Corresponding author: Lehrstuhl für Mikrobiologie, Universität Tübingen, Auf der Morgenstelle 28, D-72076 Tübingen, Germany. Tel: +49-70712972096; E-mail: karl.forchhammer@ 123456uni-tuebingen.de
                Article
                fuz025
                10.1093/femsre/fuz025
                8042125
                31617886
                64d7c646-9d03-4444-b3e1-9b9ba1acbdc8
                © The Author(s) 2019. Published by Oxford University Press on behalf of FEMS.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@ 123456oup.com

                History
                : 01 July 2019
                : 14 October 2019
                Page count
                Pages: 21
                Funding
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Award ID: Fo195/9-2
                Award ID: Fo195/13-1
                Categories
                Review Article
                AcademicSubjects/SCI01150

                Microbiology & Virology
                nitrogen assimilation,arginine synthesis,protein-serine-phosphorylation,co2 metabolism,energy sensing,2-oxoglutarate

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